川 TTERFLIES

PhilipJ. DeVries Center for BiodiversityStudies, Milwaukee PublicMuseum

Overview of Taxonomic Diversity LIKELY REPRESENT the most familiar I1. Early Stages and Host Relationships and best known group of all . Within the II1. Butterfly-Ant Symbioses context of human society, butterflies serve as center ﾂ IV. Butterfly and Diversity pieces in educational media, they are used extensively V. GeographicalPatterns of Butterfly Diversity in the arts, including nature and commercial advertis ﾂ V1. Butterfly Diversity and Habitat Destruction ing, and they are used as symbols for religious and social groups. Within the field of biology, studies on butterflies have been fundamental to the development GLOSSARY of biogeography, behavior, coevolution, conservation, development, ecological genetics, evolution,global warming, mimicry, ﾂ aposematic Describing an organism that is rendered population ecology, sexual selec tion, speciation, symbiotic associations, and systemat- less susceptible to predation by advertising its obvi ﾂ ics. In summary, butterflies have been important to ous unpalatability. Batesian mimicry A form of mimicry in which the how we perceive . target organism is rendered less susceptible to preda ﾂ tion by its resemblancein morphologyor coloration to a different that is unpalatable. 1.OVERVIEW OF BUTTERFLY cryptic Describing an organism that is concealed or TAXONOMICDIVERSITY obscured by the similarity of its appearance to the surrounding environment. Although butterflies may be the best known group of Mullenan mimicry A form of mimicry in which two insects, our understandingof their taxonomic diversity or more unpalatable species resemble each other, has two fundamentalweaknesses. The first regards the with the effect that predators are more likely to avoid recent declineof professional butterflytaxonomists and any species with this appearance. specieslevel revisions in the past 50 years. This requires myrmecophilyAbility to form symbiotic associations most species diversityestimates (from to ) with ants. to be derived from a literature that is out-0f-date. The vibratory papillae Mobile, grooved, rod-1ikeappend ﾂ second is that the number of families and of ages arising from the distal edge of the first thoracic butterfliesvaries among classificationsbecause, despite segment, used for communicating. current interest in phylogenetic systematic methodsand analyses,the relationships within the major groups are

EC ncydope mO lイ@vc ヴY 山でmel 卜 。 opyngh byACl而ade ヒミpr orights uで lionin Or血 an reserved 559 560 . BUTTERFLIES unresolved, particularlywithin Nymphalidaeand Ly- nectar, and males drink at wet soil (Fig. 1); caterpillars caenidae. Such is the state of butterfly . Never ﾂ are herbivores, body smooth without hardened spines, theless, the "true" butterflies (superfamily Papili0- and possess extrusible glands (osmeteria) that are noidea) may be placed conservatively into four families unique among butterflies; pupa typically with a silk (Papilionidae,, , and ) girdle at third thoracic segment. that together include between 12,900 and 15,819 spe ﾂ Baroniinae: one species (Baronia brevi- cies. One useful framework for organizing butterflytax- comis) endemic to ; caterpillarsunique among 0nomic diversity is P. R. Ackery's (1984) synthesis of the family by feeding on . butterfly classification, which forms the basis of the Subfamily Parnassinae: 40-50 species, mainly in followingsynopsis: north temperate mountains; host plant families include Crassulaceae, Fumariaceae,and Zygophyllaceae. Family Papilionidae (Swallowtails, Fig. I): a group Subfamily Papihoninae (Fig. I): more than 500 of 500-600 species in three subfamilies, distributed species placed into three or more tribes; distributed worldwidebut with most species being tropical;adults worldwide; most species are tropica1.Many species mediumto large sized, both sexes have six walking legs with long hindwing tails; many with sexes strongly bearing nonbifid tarsalclaws; most are brightly colored, dimorphic; many involved in mimicry; species range may be Batesian or Mullerian mimics, all feed on flower from palatable mimics (Papilioand Eurytides) to unpa1-

FIGURE1 Adult butterflies. Clockwise from upper left: (a) newly eclosed male Eurytldes protesi- 1aus (Papihomdae) drinking from wet soil; (b) male TherKas nr. hemon(Lycaenidae: ) perching on a leaf, (c) male Dismorphia amphiona(Piendae: Dismorphinae) visiting flowers; (d) female Mechanitis isthmia (Nymphalidae:Ithomnnae) ovipositing a cluster of eggs. [All photos copyright P. J. DeVnes.] . BUTTE RFLIES 561

atable models (Parides, Pachliopta, and Troides), and smal1,both sexes havesix walking legs (except Riodini- some are among the largest butterflies (.Trogonoptera nae), and frequently with alternating black and white and Omithoptera); host plant families include Annona- bands on the antennae; the group displays a tremendous ceae, Apiaceae, Aristolochiaceae, Fumariaceae,Her- diversity of form, color, and life histories; adults feed nandicaeae, Lauraceae, Magnoliaceae, Rosaceae,and on flower nectar, fruits, carrion, and honeydew, and a Rutaceae. few species do not feed as adults; some African and FamilyPieridae (whites, sulphurs, Jezebels, cabbage Southeast Asian groups are involved in mimicry com ﾂ butterflies;Fig. I): a group of more than 1100 species plexes; caterpillars most often slug-1ike, without hard in four subfamilies; adults small to medium-sized,both spines or projections, but the shows an ex ﾂ sexes have six walking legs and distinctly bifid claws; tensive variety of form; as a group, lycaenidshave the

most species are white or yellow or orange (or combina ﾂ widest･ diet breadth of all butterflies, and depending on tions thereof) derived from pterin pigments, some with the group caterpillarsmay feed on plants,other insects, red and black patterning; adults feed on flower nectar 0r insectsecretions; many caterpillarsform intimate and (Fig. 1), and males visit wet soil; caterpillars are herbi- complex symbiotic associations with ants and produce vores, body smooth without hardened spines, oftencov ﾂ acoustical calls similar to ant calls, secretions that are

ered in granulations; pupa suspended at 45 ｡ angle from harvested by ants, and chemicals that alter ant behav- substratewith silk girdle at the first abdominal segment. iors;pupae are typicallyround, seed-shaped, unadorned Subfamily Pseudopontinae:one species (Pseudopon- with projections, and may produce clicking or whirring tia paradoxd) endemicto West ; early stage biolﾂ sounds when stimulated. ogy unknown. Subfamily Riodininae (metalmarks): 1200-1400 Subfamily : approximately 100 spe- species that are almost exclusively Neotropical; argu ﾂ cies, nearly all Neotropica1. Most Dismorphia (Fig. 1) ably the most diverse of all lycaenoid groups with re ﾂ are astonishingly precise mimics of certain aposematic spect to adult and larval forms, and they are often Nymphalidae(HeHconius, Mechanitis, and Oleria), and treated as a distinct family () divided into represent the original example from which Batesian five subfamilies; adults feed primarily on flower nectar, mimicry theory was derived; host plants are in the some drink at wet soi1, others at carrion; overall their Fabaceae. life histories are poorly known, but as a group riodinid Subfamily (whites, Jezebe1, and cabbage but- caterpillarsappear to be mainly herbivores(Euselasia,

terflies): approximately 700 mostly tropicalspecies, es ﾂ Me5 山cmM ， An り @M5 ， M打 aCh& 小 ， Mぬ 伽 e， り川 mdChM ， pecially in Africa and Asia; some species have spectacu ﾂ Emesis,Anteros, and Helicopis), with a few carnivorous larly bright, contrasting colors of white, red, and black species on Homoptera (Alesa and Setabis); about (e.g., Delias, Mylothris, Pereute, and allies) suggesting one-third of the riodinids form symbioses with ants unpalatability and warning coloration; some groups and have vibratory papillae as sound producing organs with dimorphic sexes in which females resemble unpal ﾂ [Thisbe,Audre, Lemonias, Synargis, Nymphidium, and atable nymphalids and papilionids; some species un- 5etabis (Fig. 2)]; riodinid myrmecophilyis entirely dergo spectacular mass migrations (e.g., Ascia, Appias, Neotropical; host plant families include Araceae, and Belenois), and a few species are crop pests (Pieris); Asteraceae, , Bombacaceae, Cecropiaceae, host plant families include Capparidaceae, Brassicaceae, Clusiaceae, Dilleniaceae, Euphorbiaceae, Fabaceae, Santalaceae, and Loranthaceae. Lecythidaceae, Loranthaceae, Malpighiaceae, Maranta- Subfamily (sulphurs): 400-600 species ceae, Melastomataceae, Myrtaceae, Orchidaceae, Rubia- well represented in temperate and subtropical regions; ceae, Sapindaceae, and Zingiberaceae plus mosses, generally yellow or white with short, thickly scaled 1iverworts, and lichens. antennae; common in open areas, some migrate in large Subfamily Styginae: one enigmatic species (.Styxin- numbers and have been recorded out at sea far from femalis) that is endemic to the Peruvian high Andes; land (Colias, Phoebis, Catopsilia, Aphrissa, and Euremd); the early stage biology is unknown. many species with patterns visible only in the ultra ﾂ Subfamily Lipteninae: a small African group of violet. 30-40 species; some are Batesian mimics of aposematic Family Lycaenidae (hairstreaks, blues, coppers, and nymphalids (Mimacraeaand OmiphoUdotos); caterpil ﾂ metal marks; Fig. I): a group of 6000-6500 mostly lars feed on lichens and microscopic fungi (Durbania tropical species in 10 subfamilies (the total number and Deloneurd). may change with future study), and accounts for nearly Subfamily : a small group restricted to the 50% of all butterflies; most species are small to very Oriental regions; caterpillarsmay be gregarious, feed 562 . BUTTERFLIES

FIGURE2 Butterfly caterpillars. Clockwise from upper left. (a) final instar caterpillar of Morpho acfiiiies (Nymphalidae: ); (b) final instar caterpillar of Tigriciin acesta (Nymphalidae: Nymphalmae); (c) Four frames showing details of the call production mechanismof Thisbe irenea (Lycaenidae- Riodininae). Upper left@@top of caterpillar head, a vibratory papilla (arrow) and anterior margin of first thoracic segment. Upper right@@granulations on top of caterpillar head Lower left ﾑ detail of vibratory papilla. Lower right ﾑ head granulations at high magnification (d) final instar caterpillar of Thishe irenea (Lycaenidae: Riodininae) being tended by ants. [All photos copyright P. J. DeVries.]

on plants in the Fagaceae (Poritia), and may not associ- unknown; host plant families include Anacardiaceae, ate with ants. Annonaceae,Asteraceae, Bromeliaceae, Clusiaceae, Cy- Subfamily Liphyrinae: a smallgroup found in Africa, cadaceae,Euphorbiaceae, Fabaceae, Fagaceae, Gerania- Australia,and Asia; adults have the proboscis partly or ceae, Lecythidaceae, Loranthaceae, Malpighiaceae, entirely atrophied; depending on the species, caterpi1- Malvaceae, Melastomataceae, Meliaceae, Myrtaceae, lars feed entirely on insects (Homoptera) or on ant Oleaceae, Orchidaceae, Sapindaceae, Sapotaceae, S0- brood within ant nests (.Liphyraand Aslauga). 1anaceae,Sterculiaceae, Ulmaceae, and Verbenaceae. Subfamily : a moderate-sized group with Subfamily Lycaeninae (coppers): a group of 20-40 most species in tropical Africa and the Orient and one species found mainly in temperate regions, a few are in North America; caterpillarsmainly feed on nymphs tropical; caterpillars are herbivores on Polygonaceae, of Homoptera (Feniseca, 5pa!gis, and Ailotinus), with a and some form 100se associations with ants few species feeding on secretions of Homoptera Subfamily Polyommatinae (blues): a large group (AIIotinus) or ant regurgitations (Thestor); adults feed with a worldwide distribution, most are pale, reflective mainly on honeydewsecretions of Homoptera. blue above; caterpillars appear to always associate with Subfamily Curetinae: approximately 40 species re- ants, and their diets range from herbivores to cami- stricted mainly to tropical Asia, all in the genus Curetis; vores, and some (Macuiinea) feed on ant larvae and caterpillarswith tentacle organs as conspicuous, rigid are clearly complex parasites and predators within ant cylindricaltubes; caterpillars feed on Fabaceae and have nests; host plant families include Crassulaceae, Euphor- 100se associations with ants. biaceae, Fabaceae, Lamiaceae, Myrsinaceae,Oxalida- Subfamily Theclinae (hairstreaks;Fig. I): this very ceae, Primulaceae, Rhamnaceae,Rutaceae, Santalaceae, large and diverse group is found worldwide, but most Sapindaceae, Saxifragaceae, Selaginaceae, Sterculiaceae, species are tropical;caterpillars are mainly herbivores, Verbenaceae,Zingiberaceae, and Zygophyllaceae some carnivores on Homoptera, and many associate Family Nymphalidae(brush-footed butterflies;Figs with ants, but the life histories of most species remain 1 and 2): a group of 4800-6000 species in 14 subfami- . BUTTERFLIES 563 lies embracing a prodigious variety of forms and sizes, include Arecaceae,Araceae, Cyperaceae, Heliconiaceae, with both sexes having four walking legs; the forelegs Poaceae, and Selaginellaceae. are greatlyreduced (hence "brush-footed"); adults may Subfamily Brassolinae (owls): 70-80 entirely Neo ﾂ be dull brown ( and ), brightly tropical species ranging from medium to some of the colored (Nymphalinae and Brassolinae), brilliantly iri ﾂ largest butterflies known (Cflligo) that fly at dawn and descent due to physical properties of the wing scales dusk, most with characteristic,large eyespots on the (Morphinae and ), or transparent (Ithomii- hindwing underside, and they are common in butterfly nae and Satyrinae); some groups are entirelypalatable, conservatories; most species feed entirely on rotting others highly distastefu1, and some (, Ithomii- fruit juices, but a few with a stronglyreduced proboscis nae, , and Acraeinae) are extremely impor ﾂ (Brasso)isand Dynastor) may not feed;caterpillars have tant mimetic models; some species ( and smooth bodies, often with dorsal pseudospines, bifid Nymphalinae)mainly inhabit tropical forest canopies; tails, and multiple horn-1ike projections on the head; adults may feed on flower nectar, pollen, rotting fruits, host plant families include Arecaceae, Bromeliaceae, carrion, or do not feed at all; the caterpillars may bear Hehconiaceae,Musaceae, and Poaceae, and they can be many spines on the body, some also have head spines, pests in bananaand palm plantations. whereas others are devoid of spines (Fig. 2); caterpillars Subfamily Amathusiinae (fauns and duffers): an are entirely herbivorous, and the particular groups ex- Ind0-Australian group of approximately 80 species hibit strong associations with particular plant families; (sometimes placed in Brassolinae or Morphinae); me ﾂ the pupae are typically suspended. dium to large butterflies that fly at dawn and dusk Subfamily Charaxinae: a group of 350-400 mainly and feed on rotting fruit juices; the group is palatable tropicalspecies; adults fly very fast with robust bodies; (except for perhaps Taenaris) and shows little or no underside of wings typically camouflaged and leaf-1ike, mimicry; caterpillarshave smooth bodies, some with some with brilliantly colored upperside (Agrios, Pre ﾂ long, downy setae, bifid tails, often with paired head toria, and Charaxes); all are palatable,with few Batesian horns;host plant families include Arecaceae, Musaceae, mimics (Consul and Euxanthe); adults feed primarily Poaceae,and Smilacaceae. on juices of rotting fruit, dung, and/or carrion (rarely Subfamily Morphinae(morphos; Fig. 2): a group of flower nectar), and most inhabit the forest canopy; cat ﾂ 40-50 Neotropical species of mediumto very large erpillarshave smooth bodies, often bearing a corona of butterflies; the large reflective blue species (Morpho) head spines or projections; host plant families include are immediatelynoticeably in nature and in butterfly Annonaceae, Celastraceae, Convolvulaceae, Euphor- conservatories, but others that fly in the forest un- biaceae, Fabaceae, Flacourtiaceae, Lauraceae, Myrta- derstory {Antirrhea and Cflerois) are seldom observed; ceae, Piperaceae, Poaceae, Rhamnaceae, Rutaceae, San- all feed on rotting fruits, none are considered to be talaceae,and Sapindaceae. unpalatable, and none are mimics; a favorite of collec- Subfamily Apaturinae: a small group of medium to tors and butterfly conservatories, surprisingly little is large species that are mainly tropical (often placed knownof their natural history; caterpillars are covered within the Nymphalinae); males often with brilliant with red, yellow, and green patterns, bear tufts of dorsal iridescence on wing upperside,the Neotropical species and lateral setae, possess bifid tails, and bear short, (Doxocopa) with proboscis and forelegs lime-green; pairedprojections on the head (Fig. 2); host plant fami ﾂ adults are strong fliers and feed entirely on carrion and lies include Arecaceae, Bignoniaceae, Fabaceae, Men- putrefying fruits; caterpillars are herbivoreson Ulma- ispermaceae, Poaceae,and Sapindaceae. ceae and have a smooth body, bifid tai1, and head with Subfamily Calinaginae: a group represented by two a pair of strong horns. to five species in the genus Calinaga restricted to the SubfamilySatyrinae (satyrs, wood nymphs, and Himalayanregions; it is apparent that Calinaga forms browns): a cosmopolitangroup of 1500-2000 mainly mimicry complexes with Parantica (Danainae), but it tropical species that are generally dull brown (some is not clear if it is Batesian or Mullerian mimicry; cater ﾂ notable exceptions) with wel1-developed eyespots on pillars are smooth with short bifid tails and stout head the wings; most feed on juices of rotting fruits, some horns and feed on Moraceae. on fungi, and some on flower nectar in temperate re ﾂ Subfamily Nymphahnae:a diverse, cosmopolitan gions; all are palatable,with only few clear examples group of more than 3000 species (sometimes split into of Batesian mimicry from Asia (Penthema, Zethera, and Limenitinae and Nymphahnae) containing a tremen- E!_ymnios);caterpillars are smooth with bifid tails, and dous range of size and color patterns; some are migra ﾂ some bear paired head projections; host plant families tory (Vanessa,Eunica, and Sallyd), some are unpalatable 564 .BUTTERFLIES models, some are palatable mimics, some show tremen ﾂ host plant families include Apocynaceae, Asclepidaceae, dous seasonal polymorphism (Junonia), some feed on and Moraceae. flower nectar, others feed on rotting fruits and carrion; Subfamily Ithomiinae (ithomiines and glass wings; some groups inhabit tropical forest canopies (.Euphae- Fig. I): approximately300 entirely Neotropical spe ﾂ dra, Cymothoe, Panacea, Epiphile,and Baeotus), some cies; adults typically with a very small head, elongate pass north temperate zone winters as adults (Nymph- wings, and species vary in color from transparent ali5); caterpillars usually covered in spines, many with (Greta, Ithomia, and Pteronymid) to bright tiger-striped wel1-developed pairs of head spines (Fig. 2); pupa often patterns [Mechanitis,Tithorea, and Melinaea (see Fig. with bifid projections on head; host plant families in ﾂ 1)]; they are involved in both Mullerian and Batesian clude Acanthaceae, Caprifoliaceae, Convolvulaceae, mimicry, representing unpalatable models for many Euphorbiaceae,Fagaceae, Flacourtiaceae, Lamiaceae, other groups; their unpalatable properties derive from Loranthaceae, Moraceae, Plantaginaceae, Poaceae, Rub- larvalhost plants and chemicals acquired by adult feed ﾂ iaceae, Rutaceae,Salicaceae, Sapindaceae, Scrophularia- ing, and males typically possess a tuft of scent hairs ceae, Urticaceae, and Verbenaceae. between the wings that disseminate pheromones; cater ﾂ Subfamily Acraeinae: a group of approximately 250 pillars are smooth, often with fleshy tubercles, and may tropicalAfrican species, with a few in Asia and the ne0- be brightly colored or cryptic; The pupa is often retlec- tropics; ranging from small to large, all are slow-flying tive gold or silver and squat; host plant families include unpalatable species that contain cyanogenic com ﾂ Apocynaceae,Gesneriaceae, and Solanaceae. pounds, forming aposematic models for a variety of other Subfamily Tellervinae: a group of 6-10 Australasian groups, and are involved in Mullerian mimicry (, species all in the genus Teliervo;they serve as a models Bematistes, and Actinote); one species (.Acraeaencedon) for nymphahneand satyrine Batesian mimics; this is almost entirely female and reproduces via partheno ﾂ group has been included within the Ithomiinae; the genesis; caterpillars(many which feed gregariously in caterpillars resemble some Danainae and feed on Apo ﾂ communalnests) are densely covered in spines,but lack cynaceae. headspines; host plant families include Asteraceae, Pas- Subfamily Libytheinae (beaks and snout butter ﾂ sifloraceae,Sterculiaceae, Tiliaceae, and Urticaceae. flies): a cosmopolitan group of approximately 10 spe ﾂ Subfamily Heliconiinae (passionflower butter ﾂ cies recognized by the large erect palpi that form a flies): a group of 70-80 mainly Neotropical species "snout"; most species are wel1-knownto periodically with a few in Asia; most with wel1-developed eyes that undergo spectacular migrations; the caterpillars some ﾂ are wider than the thorax, elongate forewings, and most what resemble those of the Pieridae, and all feed on serve as models in Batesian and Mullerian mimicry com ﾂ Ulmaceae. plexes; they feed on flower nectar, and some on pollen ( and Laparus) from which they can derive some of their unpalatabihty; caterpillars are densely spiny, bear paired head spines, and feed entirely upon I1.EARLY STAGES AND plants in the Passifloraceae and allies ﾑ hence the name HOST RELATIONSHIPS passionflower butterflies. Subfamily Danainae (milkweed butterflies, tigers, Like all members of , butterflieshave four and crows): a cosmopolitangroup of approximately discretestages in the life cycle (egg, caterpillar, pupa, 150 species, with most in tropical Africa and Asia; rang ﾂ and the adult), each with particular characteristics, beﾂ ing from medium to large size, most are slow flying, haviors, and requirements. Furthermore,to complete conspicuously colored, and models in mimicry com ﾂ their life cycle, butterflies require a plant or host plexes (Danaus, Amauris, Idea, Tirumala, and Paran- to feed on. tica); their distasteful nature derives from feeding as caterpillarson milkweeds, but they also acquire other A・ E 既 chemical defensesby feeding as adults on flowers and woundsin certain plants containing particular alkaﾂ Butterfly eggs are laid either singly or in small to large loids; males often have wel1-developed, brush-1ike scent clusters, either on or off the host, and the location hairs they use during courtship;caterpillars are smooth, where the egg is laid is typically important (Fig. 2). 0ften patterned with alternating bands of black, white, The eggshell frequently has an elaboratesculpturing and yellow, and many have dorsal pairs of fleshy tuber ﾂ that plays a role in respiration, and each major group cles; the pupae are frequentlyreflective gold or silver; of butterfly has its own form of egg. . BUTTE RFLIES 565

B. Caterpillars Papilionidae and some Pieridaeattach by the cremaster with head upward and are restrainedby a silk girdle. Depending on the group, the appearance of butterfly Pupae of Lycaenidae produce a whirring, clicking, or caterpillarsmay range from cryptic to aposematic, they buzzing sound with a rasp and file system on the abdo ﾂ may be covered with spines and/or hairs or appear to men that may be a defense against predators. Sound be naked, and their diets may include plant tissue or production is also known in some nymphalid pupae. the flesh of other insects or they may feed entirely When mature, the pupa splits along its dorsal sur ﾂ on secretions produced by other insects (Fig. 2). All face, and the adult ecloses. After eclosion, the adult caterpillarsconsist of three major sections: the head, normally hangs from the pupal shell or nearby with the thorax,and abdomen. The hardened head houses man- wings suspended downwardso that it can expand and dibles that function to shear off bites from their food. dry its wings. If dried in a crumpledmanner the wings The head bears a gland that lays down silk that is are useless for flying, and the butterfly is effectively grasped as the caterpillar moves forward, helping the dead. As a rule, female butterflies are mated soon after caterpillar grip the substrate and also to secure rolled or even before eclosion, exemplifying one the most leavesin which they may shelter.Each thoracic segment potent laws of evolution ﾑ nature abhors a virgin. bears a pair of true legs, whereas the 10 abdominal segments form the bulk of the body, housing the long gut. Caterpillarswalk by using the prolegs (segments D ・ AduIt 3-6 and segment 10), and these function by hydraulic The adult butterfly (Fig. 1) is incapableof additional pressure and muscles. Segments 1-8 bear the external growth but is capableof flight, mating, and reproduc ﾂ ring-1ike orifices (spiracles) that allow gas exchange tion. Like all insects, the butterfly body is composedof with the atmosphere. the head, thorax, and abdomen. After reaching a particularsize eachcaterpillar instar The most obvious featuresof the butterfly head are stops eating and undergoes a molt to the next instar; the large compound eyes composedof numerous facets this is how caterpillarsgrow. Generally,but not always, (ommatidia) that cannot focus but are sensitive to there are five larval instars followed by a molt to the movement, light, and certain colors. A pair of distally pupa, or chrysalis. Caterpillar growth is not a steady thickened antennae arise from between the eyes that increase in weight from first to final instar; rather,there vary in shape according to the group. The antennae is a dramatic fluctuation of weight betweeneach molt. function as sensory organs for finding food, mating, Newly molted caterpillarsmay weigh about the same and balance during flight and are sensitive to volatile as or even less than previous instars, but their weight chemicals.Between the eyes there is a pair of append ﾂ will quickly increase and exceed that of previous instars. ages called labial palpi, and between them lie the pro ﾂ Caterpillar feeding behavior often differs among in- boscis, a hollow tube composed of two interlocking stars. In many groups, late-instarcaterpillars may stop halves that is coiled like a watch spring when not in feeding during the day and then feed entirely at night. use and can be extended for feeding. By virtue of having Alternatively,some lycaenid caterpillars may start life a proboscis, butterflies are restricted to a liquid diet feeding on plants and, after molting to a later instar, that may include flower nectar, the juices of rotting they fall off the plant, are picked up by ants, and are fruit, carrion, dung, or semidigested pollen. Proboscis carried into their nest where the caterpillars feed as lengthmay vary according to the group; in some species carnivores on ant brood. it is nearly vestigia1, thus precluding feeding as adults (Brossoiisand Liphyrd), whereas in others the proboscis measures more than 1.5 times the length of the body C ・ 而 Pa (), allowing them to take nectar from a wide When the fina1-instar caterpillar is fully grown, it stops range of flowers. eating and enters its molt to the pupa, or chrysalis. The thorax is composed of three fused segments Within the pupa the caterpillar tissues are reconstructed bearing the wings and legs, and it contains the muscles into the adult by the process knownas metamorphosis. for locomotion and various internal organs. As in all The pupa attaches to a substrate by a series of hooks on insects, the adult butterfly has six legs, one pair per the last segment (cremaster), and major groups typically segment. Butterflies have four wings (two forewings have characteristic manners of pupation. For example, and two hindwings) typically covered in scales that pupating with the head downward attached only by give butterfliestheir characteristic colors and patterns. the cremaster is typical of Nymphalidae, but pupae of The color patterns of butterflies result mainly from 566 . BUTTERFLIES the covering of scales that are arranged like overlapﾂ caterpillarshave a suite of unique adaptations that may ping roof tiles. There are three notable types of scales. include organs (collectivelyknown as ant-0rgans) to The pigmentary scales are colored by the deposition produce food secretions, volatilechemicals, and sound, of melanin, pterins, or other chemicals. Structural all of which work in concert to modify ant behavior scales generate blue, violet, copper, or green colors and enhance the protective attitude of ants toward cater ﾂ by reflecting particular wave lengths of incident light. pillars. Recent studies on ant-0rgans indicatethat myr- Androconial scales store and disseminate chemical mecophily evolved at least twice in the butterflies: once odors (pheromones) that are used in mating, and in the Riodininae and independently in other lycae- some of these scales may be physically transferred nid subfamilies. to the female during mating. The widespread trait of myrmecophilywithin the The abdomen houses the digestive and reproductive Lycaenidae and the fact that lycaenids account for ap ﾂ tracts, terminating in the reproductive organs (genita- proximately 50% of all butterfly species led Pierce 1ia).Except for segments housing the genitalia, the ab ﾂ (1984) to suggest that myrmecophily has amplified spe- domencan stretch when the gut becomesfilled with ciation rates in this group. Indeed,the diversity of life food, and abdominal distention may be considerable histories in myrmecophilous butterflies can be exceed ﾂ in groups feeding on rotting fruits (Charaxinae). The ingly complex, encompassing herbivores, carnivores, penultimate abdominal segment of males bears two ap ﾂ and those that feed as caterpillarsonly on secretions, pendages (claspers) that open to expose the aedeagus and the associations with ants range from mutualistic (penis) and serve to grip the female's abdomen during to completely parasiticor predatory. mating. The female abdomen terminates in three open ﾂ ings: the anus, egg pore, and copulatory pore. The con ﾂ figuration of genitalia is used extensively in butterfly A. Food Secretions taxonomy. Ants pay close attention to particular abdominal seg ﾂ ments bearing ant-0rgans that produce food secretions, E. Host Relationships which in some species are known to have high concen ﾂ trations ofamino acids and sugars. In some Riodininae, An important aspect in the butterfly life cycle is the these consist of a pair of organs (tentacle nectary or ﾂ ability of ovipositing females to find, and caterpillars gans) on the eighth abdominal segment that can be to feed on, particular plants. The liaison with plants extruded individually or simultaneously. In all other is so strong that many groups of butterflies only lycaenidsubfamilies, this organ is a single dorsal pore associate with particular taxonomic groups of plants; on segment 7 (dorsal nectary organ). Ants are so intent other plants are unacceptableto both caterpillars and on obtainingthe secretions that they constantly anten- ovipositing females.In the Lycaenidae this association nate the caterpillar to solicit more, and in many cases, may extend to particularspecies of ants or Homoptera. this is a good example of a generalrule among partici ﾂ For example, caterpillarsof milkweed butterflies (Da- pants in symbiotic associations ﾑ "you scratch my back nainae) only feed on plant families containing milky and I'll scratchyours." latex, and those of the Heliconiinae use plants in the Passifloraceae.Such patterns of host association in B. Semiochemical Production butterflies gave rise to Ehrlich and Raven's classic paper that developed the concept of coevolution. On Myrmecophilouscaterpillars may have extrusible the whole, host association records for the Papilioni- glands that seem to produce volatile chemicals (semi0- dae, Pieridae, and Nymphalidae are much more com- chemicals or pheromones)that alter the behaviors of plete than for the Lycaenidae attending ants. Some Riodininae have a pair of extrusi ﾂ ble glands on the third thoracic (anterior tentacle organs), whereas other lycaenidshave a pair of glands II1.BUTTERFLY-ANT SYMBIOSES on the eighth abdominal segment (tentacle organs). 1n both cases, when extruded from the body these The ability to form symbiotic associations with ants organs do not produce a liquid secretion but rather the (myrmecophily) occurs only within the Lycaenidae. tip is modified with spines that gives the appearance of Here, caterpillars provide food secretions to ants in a tiny feather duster. These spines likely provide a exchange for protection against insect predators such larger surface area to disseminate volatile chemicals as social and parasitic wasps. To form these symbioses, that may be similar to ant alarm pheromones.Instead . BUTTERFLIES 567 of anterior tentacle organs, a small group of Riodininae other ant species. Furthermore, it is in these types caterpillars(Theope) possess a corona of inflated setae of associations in which some caterpillars are adopted around the head that appear to disseminate semi0- by the ants, taken into the nest, and become parasites chemicals. or predators of their hosts.

C. Call Production IV. BUTTERFLY MIMICRY The idea that caterpillars produce acoustic calls might AND DIVERSITY seem unlikely. We now know, however, that myrme- cophilous caterpillars produce substrate-bome calls When several species of butterflies share conspicuously that function in the formation and enhancement of their bright color patterns and fly together in the same habi ﾂ symbioses with ants, and these calls bear similarities tat, this is called mimicry ﾑ a widespread and important to those produced by ants for communicating among antipredator defense.Fundamentally, mimicry occurs themselves. In most Riodininae caterpillars calls are when one species closely resembles another species, producedby a pair of mobile, grooved, rod-1ike append- and based on outward appearance one or both are ages (vibratory papillae) arising from the distal edge avoided by predators. Virtually all major taxonomic of the first thoracic segment. An acoustical signal is groups of butterflies exhibit mimicry, but the warningly produced when the grooves on the vibratory papillae colored (aposematic) models are found predominately grate against head granulations (Fig. 2). In other lycae- in particular groups of Papilionidae, Pieridae, and nid caterpillars the call is producedby thickened bumps Nymphalidae,whose caterpillars feed on poisonous located ventrally between abdominal segments. Most plants.Mimicry is a complexand subtle topic, but there concepts of insect communication suggest that acousti ﾂ are two basic types of mimicry in butterflies, both in ﾂ cal calls evolved in a sexual context. However, caterpil ﾂ volving species that advertise conspicuous color pattern lar calls provide an exampleshowing that, by forming to predators:Batesian and Mullerian mimicry. symbiotic associations, the call of one species may evolve to attract another, unrelated species. A. Batesian Mimicry This is the phenomenon whereby one or more palatable D. Ants and Caterpillar Associations species resemble one or more unpalatable model spe ﾂ cies, and the palatable species gain protection by duping In in occurs a genera1,myrmecophily caterpillars with predators.Here, predators avoid mimics because they particular type of ant. A basic element among myrme- resemble unpalatable models. The best known basic cophilous caterpillarsis that they typically form symbi- example ofBatesian mimicry involves the palatable vice ﾂ 0ses only with ant species that depend heavily on secre ﾂ roy (Limenitisarchippus) and the unpalatable monarch tions as food@@ants that also form symbioses with butterfly (Danaus plexippus)in North America. How- Homopteraand plants. Therefore, secretion-harvesting ever, Batesian mimicry occurs in all biogeographic re ﾂ ants likely played a key role in the evolution of myrme ﾂ gions, and one of the most intriguing examples involves ants are or cophily,whereas those that predators herbi- the sex-1imited mimicry of the wide-ranging African vores did not. An ecological consequence of the evolu ﾂ swallowtai1, dardanus. Here, only the females tion with secretion-harvesting ants is that in any are mimics. In this case, females are polymorphic with suitable contemporary habitat, a suite of caterpillar, respect to their appearance, and their color patterns plant, and Homoptera species all share the same species change geographically when flying with different model ant of symbionts. species. In otherwords, P. dardanus females from Kenya Among are two myrmecophilouscaterpillars there may 100k entirely different from those from Zaire or main categories of ant association. The most wide ﾂ elsewhere,and in each instance they precisely mimic a spread category comprises an association in which a different unpalatable model species. Thus, the type of particular caterpillar species may be tended by a suite female color pattern evolvesin response to and depends of secretion-harvesting ant species. The other category on the local community diversityof the model species. comprises an association in which a caterpillar has an obligate association with a single species of ant. B. Mullerian Mimicry 1n this case, female butterflies may require the presence

1e a ant species to eggs since 巧叩・ of particular lay their the phenomenon whereby several unpalatable caterpillars are unable to form symbioses with any (c0-mimics) fly in the same area and share the 568 . BUTTERFLIES same color pattern. In this case, the association of simi ﾂ ample, one might ask: Does butterfly species diversity larly patterned unpalatable species is thought to reinﾂ change with respect to latitude? or How do different force the nasty experience predatorshave when eating areas of Africa compare with respect to numbers of butterflies of such a color pattern, thus educating preda ﾂ butterflyspecies? Indeed, comparing species numbers tors to avoid it. among areas shows that latitude, biogeographical re ﾂ gion, area size, and taxonomic affinity all contribute to global butterfly species diversity.A caveat is in order C. Mimicry and Diversity about comparative species numbers: Sampling effort is among areas, Aposematic species are an important element of butter ﾂ almost always unequal different and the fly diversity, particularly in the tropics. For example, taxonomic accuracy of species counts or lists often var ﾂ approximately20-25% of all Papilionidae, Pieridae, and ies among sites. Thus, it is prudent to use care when Nymphalidaein and Kenya are clearlyapose- interpreting the generality of species diversitypatterns among areas. matic models. Although accounting for a large percent ﾂ age of all butterfly species, there are few documented examples of aposematic Lycaenidae. A. Latitudinal Gradients of Mullerian mimicry is primarily a tropicalphenome- non and is an important part of tropical faunal diversity. SpeciesDiversity This can be appreciated by considering the diversity of As is the case for most groups of terrestrial organisms, color patterns shownby many c0-mimetic speciesand butterflyspecies diversity increases toward the equator. races of ithomiine and heliconiine butterflies (plus Comparingthe North American and Neotropical faunas many c0-mimic moths and other butterfly groups) that suggests that the neotropics has an estimated 10-12 converge across large areas of the neotropics. Even times more butterfly species compared to North when the tightly overlapping distribution of only two America (Table I). Comparing site diversityat different c0-mimetic species of Heiiconius and their many pre ﾂ latitudes,however, provides a richer perspective of this cisely convergent color patterns are mappedover the phenomenon.A latitudinal transect using five wel1- Neotropical region, one cannot doubt the power mim ﾂ knownsites from the Americas makes it obvious that icry plays in the evolution,organization, and diversifi ﾂ species numbersincrease when moving from the north cation of tropical butterfly faunas. The numerous c0- latitudes toward the equator (Table II), even though mimetic species of Acraeinae butterflies throughout the the smallest areas being comparedare at the equator. African region also serve as another potent exampleof The dramatic equatorial increase in species is exempli ﾂ the influence of mimicry on the diversity of butterfly fied by the fact that a mere 500 ha of lowland Ecuadorian communities. It is clear that butterfly mimicry evolved forest has more butterfly species than all of North in the context of multispecies interactions which in- America. volved butterflies, their predators, and the plant and The relative contribution of each butterfly family to insect hosts they feed on as adults and caterpillars. site diversity also varies with latitude. From Table I1, Thus, mimicry serves to remind us that habitat distur ﾂ it is evidentthat the relative contribution of Papilioni- bance and/or destruction may have important implica ﾂ dae and Pieridae to total species diversity is about the tions for the continued survival and future evolution same regardless of latitude, but the contributions of of interacting species. Nymphalidaeand Lycaenidae increase dramatically be ﾂ

tween 20 and 0 ｡ latitude (Fig. 3). The increase in species

V. GEOGRAPHICAL PATTERNS OF BUTTERFLYDIVERSITY TABLEI ApproximateNumbers of American and World Butterfly Species One of the most freauentlyasked questions about but- North America Neotropics World terflies is the following: How many are there? The an ﾂ swer to spe ﾂ is thought be between 12,900 and 15,819 Papillionidae 35 169 621-645 a answer cies. This is hardly satisfying since the question Pieridae 63 347 1086-1105 has little biological context. In contrast, questions Lycaenidae 171 2300-3000 6000-6900 areas ﾂ framed by comparing different geographical im Nymphalidae 202 1850-2500 5175-5975 part a sense of dynamics to butterfly diversity. For ex- .BUTTERFLIES 569

TABLE11 Latitudinal Transect Showing Changes in American Butterfly Species Diversity

Family

Site Latitude Area Papilionidae Pieridae Nymphalidae Lycaenidae Total species

H. J. Andrews Forest, Oregon 44｡ 14' 6400 ha 27 23 62 Los Angeles Basin, California 34｡ 4' >1 million ha け 26 32 79 Estacion Los Tuxlas Mexic0 18｡ 35' 700 ha 4 19 113 66 212

La Selva, Costa Rica 10｡ 26' 1000 ha ] ・ 6 26 219 181 442

Garza Cocha, 0。 29' 500 ha ノ 4 L 314 312 676

cies. When averaged over the entire Table II1, the contri ﾂ bution of each family to species diversity is as follows: Papilionidae, 3.8%; Pieridae, 4.8%; Nymphalidae, 45.2%; and Lycaenidae, 46.1%. It may be significant that theseproportions approximatelyreflect those observed when comparing latitude (Fig. 3). Comparisonsamong sites from the Americas point to the general relationship of the higher species richness that occurs at lower latitudes and to the marked varia ﾂ tion among sites that share many species in common. These examples also show that the relative contribution of each family to species richness is not equal; the proportion of nymphalid and lycaenid species increases toward the equator, but the proportion of papilionid and pierid species appears relatively constant. At this point, we might ask if there are similar patterns outside the neotropics

C. Regional Patterns of Species Diversity

Although most butterfly species are tropica1,the num ﾂ ber of species is not distributed equally among tropical regions (Table IV). As one might expect, those areas closest to the equator have a greater number of species, but there is also an effect of size on species diversity (Table IV). In this comparison, the continent of Africa has by far the most species, but it also encompasses the greatest geographical area and habitat types (deserts, mountains, forests, and savannas) of any area. Within Africa there are more species in Zaire than in Kenya or Southern Africa, highlighting the ecological diversity in African climate and habitat types. Thus, the entire continent of Africa should contain more species than a geographic subset. As in the neotropics, the relative contributions of families to total species numbers differ among areas of Africa(Table IV). Here, the Papilionidae and Nymphali- dae contribute equally to total richness of both Kenya 570 , BUTTERFLIES

TABLEIII

Comparative Diversity among Neotropical Sites"

Family

Site Papiliomdae Piendae Nymphalidae Lycaenidae Total species Total area (ha)

246687104u Estacion Los Tuxlas Mexico 14 (6.6) 19 (8.9) 113 (53.3) 66 (31.1) 700 り花 Finca La Selva, Costa Rica 16 (3.6) 26 (5.8) 219 (49.5) 181 (40.9) 1,000

Garza Cocha, Ecuador 25 (3 ・ 乃 315 (46.6) 312 (46.1) 24 (3.5) 卯口卯卯丑四 500 Jatun Sacha,Ecuador 25 (3.6) 23 (3 2) 306 (43.7) 345 (49.3) 600 Paquitza, Manu, 25 (2.9) 31 (3 6) 369 (43 3) 427 (50.1) 3,900 Tarnbopata, Peru 25 (3 1) 26 (3 3) 337 (42.3) 409 (51.3) >2000

Cacaulandia, 30 (2.5) 31 (2.6) 423 (35.3) 715 (59.6) 2,000 AltoJurua, Brazil 38 (3.7) 37 (3.6) 467 (45.0) 496 (47.8) >500 Cerro do Japi, Brazil 19 (4.7) 36 (8,9) 193 (47.8) 156 (38.6) >400

｡ The percentage of the total species at a particular site is in parenthesis

and Zaire, but Kenya shows an increasedproportion of fauna of Madagascar is interesting. Here, only 17% of Pieridaeand a decreased proportion of Lycaenidae. On all butterflies are lycaenids,but nymphalids constitute the other hand, the proportional contributions of Papili- 67% of the total fauna, most of which are Satyrinae 0nidae and Pieridae are reversed in the Zaire fauna. The (i.e., 42% of all the butterflies). This example demon ﾂ Papilionidae and Nymphalidae in the Southern African strates how historical colonization and subsequent radi ﾂ fauna contributeless to the total than other mainland ation of an island by one group can produce a fauna African areas, but nearly 55% of all Southern African distinctly different in composition from that of the butterflies are Lycaenidae. Overal1,these proportional mainland. differences (Table IV) may reflect the ecological re ﾂ Only a broad-brush comparison among areas of dif ﾂ sponses of taxonomic groups to differences in habitat ferent sizes and regions is necessary to appreciate that, types and/or the differences among regional taxon0- 0veral1,butterfly diversity is highest in the neotropics mists. Finally, in comparison to mainland Africa the (Table 1-Table V). Despite the great disparity in ge0-

TABLEIV

Variation in the Contribution of Each Family to Species Richness among Different Faunas'

Family

Fauna Papilionidae Piendae Nymphalidae Lycaemdae TO口 l

All ・ of Africa 80 (2.9) 145 (5.3) 1107 (40.6) 139 ア (51 ・ 2) 2729 Zaire 48 (3.7) 100 (7.6) 607 (46.5) 551 (42.2) 1306 Kenya 27 (3.7) 87 (12.1) 335 (46 5) 271 (37.6) 720 Southern Africa 17 (2.3) 54 (7.2) 265 (35.6) 409 (54.9) 745

Madagascar 13 (4.9) 28 て 10 ・ アり 175 (66.8) 46 (175) 262 Australia 18 (6 5) 35 (126) 85 (30 6) 140 (50 3) 278 New Guinea 41 (5 2) 146 (18 6) 222 (28.3) 376 (47.9) 785 Malaysia 44 (5 8) 44 (58) 273 (35.9) 400 (52 5) 761 Costa Rica 42 (4 0) 71 (6 8) 438 (41.9) 493 (47 2) 1044

' The percentage of total faunal richness by each family is given in parentheses . BUTTERFLIES 571

TABLEV Percentage of World Species by Geographical Region"

Reeion

North America Neotropics Costa Rica Africa Australia New Guinea Maylasia

Total species 471 5341 1044 2729 278 785 761 ・ ・ % World fauna 3・ 4 38 8 7・ 6 19 ・ 8 2・ O 5 ・ 7 う・ 5

｡ Total number of butterfly species for world fauna (13, 753.5) and the neotropical region (5341) represent averages

fy

U 川川別川川川川川川川 十斗8 七レ月巳ヨL z LSmrd6dut 0 川M Q必二十川刑刊刊M 十卜-ヰ o卜H トリハM yrdnn2つ 川 M 6 卜 mm・ ReFduE((MLmMUCe vanaMonthly teOd ni py he ness (top an d北 H卜 什 丁 DeVries(fromom)offruit-fe 叫 41LgL inf orestc an 叩yLd 572 .BUTTERFLIES

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FIGURE5 Species diversity of fruit-feeding Nymphalidaeshowing the relationship to space and sample-size. Each numberedline represents a plot sampled from within a single tract of continuous rainforest (from DeVries et a1., 1999).

V1.BUTTERFLY DIVERSITY AND Acknowledgments HABITATDESTRUCTION The author is indebted to P. Ackery, G Austin, G Beccaloni, S Collins, H. Greeney, A. Heath, R. Hil1, R. Lande, T. Larsen, D. Lees,

plant and/or insect hosts, c0-mimics in Batesian and Mullerian mimicrycomplexes, predators,and parasites. See Also the Following Articles

Butterfliesgreatmanyhave biomes, also habitats,evolved and within microhabitats, and adapted rangingtoa HYMENOPTERACOEXISTENCE ･ INSECTS,OVERVI'IEW ･ MOTH ･ SPECIES from the multilevels within lush tropical rain forests to starkly dry deserts and subarctic tundra. Habitat destruction always has profound effects on Bibliography the biological communities that inhabit them, and but- Ackery, P. R. (1984), Systematic and faumstic studies on butterflies terflies are no exception. Like all organisms, butterflies Symp. R. Ent. Soc. 11, 1-21

Their Cladisticsand Biology. British Museum (Natural History), terflies have served as tools for understanding the diver- London Sification of life on Earth and the fundamental in- Beccaloni, G. W (1997a). Vertical stratificationof ithomiine butterfly teractions among species. However, our future (Nymphalidae:Ithomiinae) mimicry complexes: The relationship understandingrenewedinterestofinbutterflystudying diversitythem inwillthe natural depend world on a Corbet, betweenLinnean A. S.,SocadultPendlebury, 62, flight 313-341. height H M., and Eliot,larval J. host-plantN. (1992). height. The ButterfliesBioi.]. and valuing the habitats in which they occur. of the Malay Peninsula MaylayanNature Society, Kuala Lumpur.