Feeding Mechanisms of Adult Lepidoptera: Structure...

ANRV397-EN55-17 ARI 2 November 2009 12:12

Feeding Mechanisms of AdultLepidoptera: Structure,Function, and Evolutionof the MouthpartsHarald W. KrennDepartment of Evolutionary Biology, University of Vienna, A 1090 Vienna, Austria;email: [email protected]

Annu. Rev. Entomol. 2010. 55:307–27

The Annual Review of Entomology is online atento.annualreviews.org

This article’s doi:10.1146/annurev-ento-112408-085338

Copyright c© 2010 by Annual Reviews.All rights reserved

0066-4170/10/0107-0307$20.00

Key Words

proboscis, fluid uptake, flower visiting, feeding behavior, insects

AbstractThe form and function of the mouthparts in adult Lepidoptera andtheir feeding behavior are reviewed from evolutionary and ecologicalpoints of view. The formation of the suctorial proboscis encompasses afluid-tight food tube, special linking structures, modified sensory equip-ment, and novel intrinsic musculature. The evolution of these function-ally important traits can be reconstructed within the Lepidoptera. Theproboscis movements are explained by a hydraulic mechanism for un-coiling, whereas recoiling is governed by the intrinsic proboscis mus-culature and the cuticular elasticity. Fluid uptake is accomplished bythe action of the cranial sucking pump, which enables uptake of a widerange of fluid quantities from different food sources. Nectar-feedingspecies exhibit stereotypical proboscis movements during flower han-dling. Behavioral modifications and derived proboscis morphology areoften associated with specialized feeding preferences or an obligatoryswitch to alternative food sources.

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Plesiomorphic:character of ancestralcondition, presentbefore the lastcommon ancestor ofthe taxon

INTRODUCTION

The Lepidoptera (butterflies and moths) areone of the most diverse taxa of animals contain-ing about 160,000 described species in 47 su-perfamilies (103). Both the larval and the adultstages of nearly all species are associated withvascular plants. Most larvae feed on plant mate-rial using biting-chewing mouthparts. The ma-jority of adults are anthophilous; they possessa proboscis that is used to imbibe floral nec-tar and other liquid substances. The role ofLepidoptera as pollinators has been demon-strated in many cases of mutualistic relation-ships with flowers and floral specialization (59,79, 113, 125, 128). Their adaptation to flowermorphology provided classical examples of re-ciprocal adaptations in insect-flower interac-tions (36). After Charles Darwin examined theflower of a star orchid possessing an approxi-mately 300-mm-long nectar spur, he predictedthe existence of a hawk moth with a proboscis ofmatching length (36) that was actually discov-ered 40 years later (114). The fossil record ofLepidoptera dates back to the Jurassic period,yet the evolution of present-day species-richlineages are probably related to the radiationof angiosperms during the Cretaceous withina relatively short time frame (145). The shiftof larval feeding to angiosperm foliage couldhave been crucially linked with the evolution ofadult nectar feeding and the adaptive radiationof glossatan Lepidoptera (136).

The mouthparts of Lepidoptera belong toone of the best-studied feeding organs offlower-visiting insects, in terms of anatomy,functional morphology, and evolutionary bi-ology (91). Several benchmark morphologicalstudies, dating from the latter half of the twen-tieth century, led to the establishment of a phy-logenetic classification of the major lineagesof Lepidoptera that was strongly supportedby arguments regarding mouthpart structures(38, 95, 101, 112). This high-level classifica-tion, based on morphology, has remained ro-bust in light of present-day molecular-basedphylogenies (62, 146). The anatomy of thelepidopteran mouthparts has been reviewed

comprehensively in a phylogenetic context (96,98, 103). Here, I focus on the evolution of func-tionally important traits of the proboscis, themechanisms of proboscis movements and fluiduptake, as well as feeding behavior on flowersand adaptations to other food sources.

COMPOSITION ANDEVOLUTION OF LEPIDOPTERANMOUTHPARTS

Biting-Chewing Mouthpartsin Adult Lepidoptera

The origin of the lepidopteran proboscis canbe traced back to the pair of small galeaeof uncertain function in the plesiomorphicbiting-chewing mouthparts retained in non-glossatan moths of the families Micropterigidae(Figure 1), Agathiphagidae, and Heterobath-miidae (54, 72, 87, 95, 98, 140).

The Micropterigidae possess a complete setof mouthpart structures that are well adaptedfor collecting and grinding angiosperm pollenor fern spores (33, 72, 97, 140). Covered by thelabrum, the asymmetrical mandibles act like amortar and pestle to crush pollen grains. Themaxilla consisting of cardo and stipes gives riseto the small lacinia on the median side, as wellas the short galea and the large, five-segmentedmaxillary palp (Figure 1a). The galea isequipped with microtrichia, a row of lamellatesetae, few uniporous sensilla, and bristle-shapedsensilla, as well as one small muscle attached tothe stipes (33, 53, 72, 88). The maxillary palpscrapes pollen out of anthers (72). Pollen grainsadhere to the paddle- and mushroom-shapedbristles of the apical segment (Figure 1b),which transport the pollen to the mandibles(33, 53). The labium bears a pair of shorttwo-segmented labial palps, which bear apicalsensory pit organs (33). Species of Micropterixfeed on a variety of flowers (97), whereasthose of Sabatinca usually feed on pollen ofZygogynum (Winteraceae) flowers, which arepollinated during the search for pollen (138).These moths use paddle- and spatula-shapedsensilla for pollen collecting (55). Whether

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lplp

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gaga

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Figure 1Head of Micropterix aruncella (Micropterigidae) (scanning electron micrographs) illustrating the plesiomorphic biting-chewingcondition of mouthparts in adult Lepidoptera. (a) The labrum (lr) covers the mandibles. The maxilla bears the galea (ga) and thefive-segmented maxillary palp (mp). The labium bears a pair of two-segmented labial palps (lp). (b) Concave short galea (ga); apicalsegment of the maxillary palp (mp) is equipped with mushroom-shaped sensilla for the uptake of pollen grains.

adults of the Agathiphagidae feed at all is un-certain; nonetheless, their mandibles are usedto open the pupal casing for emergence (97).Adult Heterobathmiidae frequent flowers ofNothofagus (Nothofagaceae) to feed on pollen;in addition, they have been observed to drinkwater (102). Their mouthparts are similar tothose of the Micropterigidae (99) and are welladapted to collect and grind pollen, but onlyone type of so-called prehensile sensilla occurson the maxillary palp, where pollen and fernspores are frequently found (54).

Mouthparts of Glossata and Evolutionof the Proboscis

The great majority of adult Glossata possessa coilable proboscis (Figure 2), which evolvedonly once, thus representing an autapomorphyof this clade. Adult Glossata take up only liquidfood and achieve this exclusively by way of thefood tube of the proboscis, which is composedof the medially concave and interlocked galeae.The origin of the proboscis and the transition tofeeding on liquids resulted in the reinforcementof the sucking pump in the head and a reduction

Autapomorphy:derived character,unique to a taxon

Glossata: taxon ofLepidopteracomprising more than99% of species;characterized by thecoilable proboscis,among other traits

Ditrysia: taxon ofLepidopteracharacterized byspecialized femalegenital apparatus

of all major constituents of the mouthparts, ex-cept the galeae and the labial palps (136). Theother components of the mouthparts play norole in food uptake but may have sensory func-tion during foraging.

In species with a functional proboscis, thelabrum forms a small plate over the basal pro-boscis joint, where bristles of the pilifers con-tact the basal galeal joint; these sensory bristlesprobably detect proboscis movements (53, 84,87). The mandibles are reduced and nonfunc-tional. The basal maxillary sclerites—the stipesand the cardo—form a tubular component fromwhich the coilable galea and the maxillary palpemerge (Figure 2b); a lacinia is absent (98).

The maxillary palps are composed of fivesegments in the plesiomorphic condition,but are short and reduced in the number ofsegments in most species of Ditrysia (98). Thebiological role of the maxillary palps remainsunclear despite the presence of sensilla in var-ious lineages (52, 53, 57). In the females of theyucca moth, Tegeticula and Parategeticula (Pro-doxidae), the second segment of the maxillarypalpus is extended into a long coilable tentaclethat is used to collect pollen and to actively

www.annualreviews.org • Feeding Mechanisms of Adult Lepidoptera 309

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100 µm100 µm100 µm500 µm500 µm 10 µm10 µm500 µm 10 µm

pdldl

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Figure 2Head of the butterfly Vanessa cardui (Nymphalidae) (scanning electron micrographs). (a) The proboscis (p) is coiled in the restingposition; one labial palp (lp) is shown (the other one has been removed). (b) The pilifers (pi) contact the basal proboscis. The galea (ga)extends from the foldable stipes (st) and bears the minute maxillary palp (mp); the arrow points to tip region. (c) The tip region ischaracterized by sensilla styloconica (sst) and slits between the dorsal linking structures (dl).

pollinate Yucca flowers (37, 119). The tentaclesare as long as the proboscis and are similarlyequipped with muscles and sensilla. This ex-traordinary and novel organ probably evolvedas an adaptation to the mutualistic pollinationbehavior of female yucca moths (120).

The labial palps are composed of two tothree segments (98). They extend from theprementum sclerite and may form prominentstructures in front of the head (Figure 2a).They are equipped with scales, bristles, and var-ious sensilla partly arranged in an apical pit or-gan (52, 53, 57, 98). The sensilla of the pit or-gan are sensitive to carbon dioxide (25, 68, 78,106). They play an important role in the nectar-foraging behavior of sphingid moths (139). InManduca sexta (Sphingidae) the labial pit organ

detects minute changes in concentration of car-bon dioxide, which serves as a distant olfactoryattractant to freshly blossomed flowers (65) andas a predictor of nectar volumes before actualflower probing (67).

The plesiomorphic condition of the pro-boscis occurs in the representatives of the familyEriocraniidae, which use their short and sim-ply composed proboscises to drink from waterdroplets and sap seeping from injured leaves(93, 95). Originating from the tubular stipes,the coilable galeae are linked to each other bypointed cuticular structures on the dorsal andventral sides of the median food canal. Theouter surface of each galea bears microtrichia,few uniporous sensilla basiconica, and bristle-shaped aporous sensilla trichodea. The galeal

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lumen contains a nerve, a trachea, and an extrin-sic muscle that originates on the stipes; how-ever, no intrinsic galeal musculature extends tothe tip (87, 88, 93).

Derived from the plesiomorphic condition,the proboscis of Myoglossata is characterizedby functionally specialized dorsal and ventrallinking structures, three morphological typesof sensilla, and additional intrinsic galeal mus-cles (87, 88, 101). The principal composition issimilar in Myoglossata, except for the species-poor family Neopseustidae, in which each galeaforms a functionally closed food tube. The shortdouble-tube proboscis is held together by spe-cial scales that extend from the ventral side ofeach galea. The galeal lumen contains a slen-der intrinsic galeal muscle in addition to thebasal extrinsic muscle (88, 100). Three typesof proboscis sensilla are present, including sen-silla styloconica (56, 57), which was previouslyregarded to be restricted to the nectar-feedingtaxa (87). The food source of the neopseustidmoths is still unknown.

The proboscis of the Eulepidoptera exhibitsfeatures that probably evolved in context withflower visiting: considerable length, complexlycomposed galeal walls, a fluid-tight food tubewith a special tip region, and numerous intrin-sic galeal muscles (Figures 2, 3) (87, 88). Theproboscises of nectar-feeding species display

Myoglossata: taxonof Glossatacharacterized byintrinsic proboscismusculature

Eulepidoptera:primary nectar-feedingLepidoptera

amazing lengths, which range between 3.5 and49.9 mm in butterflies (104) and between 2.5and 280 mm in sphingid moths (4, 109). Inbutterflies the length normally corresponds toabout 43–93% of the body length (34, 104, 118).In the family Sphingidae the body mass is posi-tively correlated with proboscis length (2). Dis-proportionately long proboscises exceeding thebody length occur in some species of the Hes-periidae, Riodinidae, and Sphingidae families.The current record holder among true butter-flies is Eurybia lycisca (Riodinidae), with a 49.9-mm-long proboscis, about twice as long as itsbody (104). The longest proboscis yet encoun-tered in any flower-visiting animal belongs tothe Neotropical hawk moth, Amphimoea walk-eri, and measures 280 mm (4).

The proboscises of nonfeeding adult Lep-idoptera are generally more or less reducedin length and structural complexity (130), butdetailed studies are lacking. Reduced pro-boscises are characteristic of the representativesof the superfamilies Hepialoidea, Tineoidea,Cossoidea, and Lasiocampoidea. Furthermore,rudimentary proboscises are occasionally en-countered in species of other taxa, such as theSesioidea, Pyralidoidea, Bombycoidea, Noc-tuoidea, and Geometrioidea (98, 130). All truebutterflies, the Papilionoidea, possess a fullyfunctional suctorial proboscis.

dl

vl

t

nn

mimmim

limlim n

mim

limmimmimmim

bgmbgmbgmft

100 µm100 µm

ba

Figure 3Proboscis anatomy of the butterfly Vanessa cardui (Nymphalidae). (a) Longitudinal section through the basal joint region shows thebasal galeal muscle (bgm) and the median intrinsic muscle (mim). (b) The lumen of the galea contains a trachea (t), nerves (n), and twoseries of muscles, the median intrinsic muscles (mim) and the lateral intrinsic muscles (lim). The food tube (ft) is closed by theoverlapping dorsal linking structures (dl) and the ventral linking structures (vl), which are hooked with their counterparts.


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Macrolepidoptera:medium to large,broad-wingedLepidoptera withexophagous larvae

The composition of the galeal wall ensuresthe elasticity for coiling and uncoiling withoutdeformation of the food tube. The outer galealwall is composed of darkened cuticle rings thatlie embedded in the lighter-hued cuticle, givingthe proboscis an annulated appearance (73, 82,118). The dark cuticle is probably hard exocu-ticle, whereas the light cuticle is interpreted toconsist of flexible mesocuticle and endocuticle.Resilin is found in particular areas of the pro-boscis wall (73). In many species, distinct ribs,visible on the convex outer surface, may havecuticular spines, hair-like cuticular processes, orscales (82, 87, 118, 134). The concave mediansurface that forms the food tube is composed ofsmooth plates that may be vertically fluted (73,87, 118).

The galeae are held together by rows of in-terlocking cuticular processes, termed legulae,that exhibit different shapes on the dorsal andventral sides of the food canal (Figure 3b) (44,73, 87). The dorsal linkage consists of flat hor-izontally extending lancet-shaped plates. Theyoverlap those of the opposite galea to form theroof of the food tube. Their principal varia-tion in Glossata concerns the number of rows(87). Single-celled glands are situated in thegaleal epidermis and empty toward the dorsallegulae; their secretion serves to lubricate andseal the dorsal linkage in butterflies (44). Tworows of ventral legulae are plesiomorphic inEulepidoptera; in certain lineages of Ditrysiathe lower legulae are modified into hooks thatinterlock with their counterparts, like a zip-per (Figure 3b), providing firmness to the pro-boscis linkage (87).

Dorsal and ventral linking structures sealand firmly link the food tube; they are re-garded as a functional precondition for a sucto-rial proboscis that takes up fluid along a pres-sure gradient (28). The fluid-tight food tubenecessitates a specialized region for fluid intake.Near the tip, the dorsal legulae are particularlyelongate and between them are drinking slits,which permit the uptake of fluids (Figure 2b,c).This region comprises 5–20% of the proboscislength in butterflies (92, 118, 123). Nymphalid

butterflies and probably all other Macrolepi-doptera assemble their proboscises after emerg-ing from the pupal stage, because the galeae de-velop separately from each other. This behav-ioral process renders the proboscis functionaland has to occur immediately after eclosion(83).

The sensory equipment of the proboscis wascomprehensively reviewed by Faucheux (53).The sensilla trichodea or sensilla chaetica havean aporous sensory bristle that extends from acollared socket. They occur only on the exter-nal surface of the proboscis and become shorterand more scattered toward the tip; in most but-terflies they are longer on the ventral side of theproboscis than on the dorsal side (84, 118). Onthe basis of ultrastructural studies, these sen-silla are regarded as mechanosensitive (5, 84).They might provide information on the widthand depth of tubular flowers during probing(84). Flower-handling efficiency relies heavilyon mechanosensory input, as shown for speciesof sphingid moths (66). Bristle-shaped sensillaprobably also provide tactile information con-cerning the correct resting position of the pro-boscis, as scanning electron micrographs con-firm that they contact the surface of the adjacentcoil (82).

The sensilla basiconica of the external pro-boscis surface are arranged in irregular rows,whereas in the food canal they form a singlerow (52, 75, 84, 87). They consist of a shortdome-shaped socket and sensory cone that maybe elongate or short, blunt or sharply tipped;sometimes it barely extends beyond the surfacesculpture of the galeal wall (3, 5, 52, 53, 84, 118,123, 131, 141). A terminal pore may be presentor absent; in exceptional cases the cone is multi-porous (53). Deduced from their ultrastructure,these sensilla are regarded as chemo- and/ormechanoreceptive (84, 135, 141). In electro-physiological tests, the sensilla of the food canalrespond to sucrose solutions (75) and may pro-vide information on flow rates by means of gus-tatory cues received from the imbibed fluid (84).In addition, sensilla ampullacea occur near theproboscis tip in the Sphingidae (53).

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The sensilla styloconica are composed of avariously shaped stylus and a shorter terminalsensory cone (Figure 2c). Sensilla styloconicaare regarded to be derived from sensilla basi-conica (3, 53, 131) and do not occur in non-glossatan Lepidoptera (87). They are arrangedin one to three regular rows in the distal halfof the proboscis and are restricted to the tipregion, where the drinking slits occur in but-terflies (84, 87, 118, 123, 131) and in the noc-tuid moth Heliothis virescens (105). Their num-ber may range from 7 to 144 per galea andtheir length from 10 to 237 μm in butterflies(53, 118, 123). An astounding diversity of sen-silla styloconica lengths and shapes are found intaxa of the true butterflies (the Papilionoidea)and the families Noctuidae, Geometridae, andPyralidae. Cross-sections reveal the stylus tobe either smooth and ellipsoid or longitudi-nally ribbed and star-shaped; some species ex-hibit terminal spines around the sensory cone,whereas in others the ribs are serrate or veryshort and practically absent (52, 53, 84, 87, 92,105, 118, 123, 131, 141). In species of the Sph-ingidae the short sensilla styloconica are locatedin pits and never extend beyond the surface ofthe proboscis (53). Comparative morphologi-cal studies suggest that a stylus with cuticularridges is the plesiomorphic condition in Glos-sata (57, 87). Derived sensilla shapes evolvedin adaptive context with derived feeding habits(32, 92, 110). The internal ultrastructural com-position is similar in all examined taxa despitethe variety of external shapes. The sensory coneis uniporous; in some species wall pores werealso detected. Each sensillum contains three tofour receptor cells with dendrites extending tothe terminal pore. One dendrite ends with atubular body at the base of the cone, indicatingthat the sensillum serves as a combined chemo-and mechanosensory organ (3, 84, 105, 111,141). Sensilla styloconica are sensitive to cer-tain mono- and oligosaccharides and a variety ofother substances (22, 127). For example, in but-terflies that feed on fermenting fruits, the sen-silla also respond to ethanol (117). The centralprojection pattern of the sensory neurons can

be divided into two categories, which presum-ably reflect the functions of these sensilla (105).The axons of the receptor neurons enter thetritocerebrum and terminate near the antennalgustatory neurons. Stimulation of sensilla stylo-conica with sucrose increases proboscis move-ments and food ingestion (76).

In species of Myoglossata, the galeal muscu-lature consists of extrinsic and intrinsic galealmuscles (88, 101). The extrinsic galeal mus-culature, i.e., the basal galeal muscle, origi-nates near the stipital-galeal junction and ex-tends into the basal galea (Figure 3a). The in-trinsic galea musculature extends in the galeallumen distal from the base (Figure 3b) andis regarded as a functional adaptation that en-ables the lengthy proboscis to perform its char-acteristic flower-probing movements. A hypo-thetical pathway proposes four key events forthe evolution of novel proboscis musculature:(a) the recruitment of muscles from the basalgaleal muscles by shifting the attachment sitebeyond the basal joint, (b) the shift of themuscle origin site into the galea resulted inthe intrinsic galeal muscles in species of Eu-lepidoptera; followed by (c) the multiplicationof the musculature in context with probosciselongation in the lineage of Ditrysia. (d ) Thesplit into two series of overlapping musclesresulted in a more dense arrangement of in-trinsic musculature as found in most mem-bers of Apoditrysia as well as all Macrolepi-doptera, including butterflies (Figure 3b)(88, 89).

FUNCTIONAL MECHANISMS OFPROBOSCIS AND FLUID UPTAKE

Movements of the Proboscis

Compared with the proboscis of other nectar-feeding insects, the proboscis of Lepidopterahas several unique features. It forms a flat,vertical spiral when at rest (Figure 2a), it con-sists of merely two components, and it func-tions primarily by means of a hydraulic mech-anism (82). How the proboscis works has long


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been a source of controversy (7, 44, 94, 129).Comparative and experimental studies (7, 82,85, 142) provide strong evidence that the samemechanisms of movements operate in all speciesregardless of proboscis length or the variousarrangements of galeal muscles or behavioraladaptations to particular food sources.

In the resting position the proboscis is coiledinto a spiral of 2.5 to 7 turns (82, 94). The pro-boscis is tightly wound onto itself so that thereis no space between the coils. It lies againstthe labium (Figure 2a) between the labial palps(82).

The uncoiling process relies on a hydraulicmechanism (7, 82, 129, 142). The proboscis isfirst unlocked from its resting position—it iselevated by the basal galeal muscle. Owing toits elasticity, the coil of the proboscis loosenssomewhat. Further uncoiling is enabled by con-traction of stipes muscles, whereby movementsof the sclerotized part of the stipes compress thestipital tube (Figure 4a). The repeated com-pressions of the stipes force hemolymph intothe attached galea. Because the structures of thestipes form a valve, the proboscis is stepwise un-coiled when the hemolymph pressure inside the

a b

esm

bgm

ism

igm

Figure 4Functional mechanisms of the proboscis movements in Lepidoptera. Schematic illustration of a lateral viewof an opened head. Arrows indicate direction of proboscis movement; contracted muscles are shaded red.(a) Hydraulic mechanism of proboscis uncoiling. External stipes musculature (esm) compresses the tubularpart of the stipes (blue arrowhead ) and pumps hemolymph into the attached galea. Basal galeal muscle (bgm)elevates the proboscis. (b) The coiling process involves contractions of the intrinsic galeal muscles (igm) andproboscis elasticity; contraction of internal stipes muscle (ism) flexes the proboscis into the resting position.

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galeae increases. The increased internal pres-sure results in an outwardly arched dorsal wallin the uncoiled proboscis (85). The uncoiledproboscis normally assumes a bent positionwith a more or less distinct flexion, termed thebend region or knee-bend (Figure 5a) (7). Thebend region is probably caused by the elasticityof the proboscis (82, 85). Increased hemolymphpressure can lead to a nearly straight position ofthe proboscis; in some cases, the distal proboscisbends slightly upward (7, 143). During flowerhandling, the proboscis is elevated by contrac-tion of the basal joint muscles, while forward orbackward movements of the region distal to thebend region (Figure 5a) are caused either by anincrease in pressure due to stipital pumping orby action of the intrinsic galeal musculature ofthe proboscis, respectively (82).

After the stipes valve opens, proboscis coil-ing is achieved by the elasticity of the cuti-cle, which loosely recoils the spiral into 1.5to 2.5 turns. The contractions of the intrin-sic galeal muscles (Figure 4b) are responsi-ble for tightening the coil as indicated by ex-periments and electromyogram recordings (85,142). The final resting position is achieved afterthe coiled proboscis has been flexed under thehead by contraction of a single stipital muscle(Figure 4b). Presumably, after relaxation of theintrinsic galeal muscles, the proboscis unwindsslightly until it contacts the labium (82). Thesculpture and cuticle processes of the probosciswall provide the grip needed to hold the coiledproboscis under the head without further mus-cular contraction, and microtrichia on the me-dian sides of the labial palps are hypothesizedto assist in fixing the final position (82, 91).

Capacity of Fluid Uptake

Glossatan Lepidoptera take up fluid along apressure gradient in the food tube of the pro-boscis that is created by a sucking pump in thehead. A biophysical model based on the Hagen-Poiseuille equation shows that the flow rateis proportional to the pressure drop producedby the sucking pump and the diameter of thefood tube, but it is inversely proportional to

proboscis length and viscosity of the fluid,which depends on the sugar content (80). Thismodel predicts an optimal nectar concentrationof 30–40% sucrose to maximize energy intakein butterflies and hawk moths (35, 77, 107).In natural habitats, however, flower choice de-pends on additional parameters such as avail-able nectar concentration and volume, flowermorphology, availability and density of flowers,as well as handling and transit time betweenflowers (23, 28).

The capacity of the feeding apparatus is bestmeasured by uptake volume during feeding ex-periments. The volume of fluid ingested bynymphalid butterflies varies from 36–133 μl ofartificial nectar depending on body size (70, 81,110). Under near-natural conditions the mealsize of Vanessa cardui was 28 ± 9.3 μl (S.D.),in which an average of 145 ± 56 flowers wereprobed in 48 ± 24 min, with an average vol-ume rate of 19.3 ± 10.4 nl per second (70).Stimulated V. cardui butterflies consumed arti-ficial nectar (30% sucrose) from artificial flow-ers, which is equivalent to an average of 15.23%of its body weight within 2 min, or it consumedmean nectar amounts, which are equivalent to41.6% of its body weight when feeding untilsatiation (81). The larger sized Morpho pelei-des consumed nectar equivalent to an averageof 23.6% of its body weight within 2 min andequivalent to 43.7% of its body weight in ap-proximately 10 min. The uptake of highly vis-cous sugary fluids from rotting fruits probablyinvolves a dilution of the sugar with salivaryfluid (81). An oral valve permits an alternatingflow of saliva and nutritive fluid through thefood tube (46).

Tropical hawk moths consume between 0.4and 1 g of nectar per night (143). Their aver-age meal size decreased linearly with increasedsugar concentration, from 0.35 g at 10% to0.11 g at 50% (137). The intake rate of hawkmoths was analyzed as a function of sucrose vis-cosity (by adding tylose as an inert polysaccha-ride) in a 30% sucrose solution. Because theintake rates decreased with increasing viscosity,it was concluded that the gustatory input effectsfluid ingestion independent of viscosity (77).


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a

100 µm100 µm100 µm 100 µm100 µm100 µm 100 µm100 µm100 µm

d

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b

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e

100 µm100 µm100 µm

f

c

Figure 5Examples of Lepidoptera feeding on various food sources (arrows indicate proboscis movements) and corresponding characteristicproboscis morphology (scanning electron micrographs). (a) A nectar-feeding butterfly, Argynnis paphia (Nymphalidae), possesses aslender proboscis tip. (b) A pollen-feeding butterfly, Heliconius pachinus (Nymphalidae), with a load of pollen on the proboscis. (c) Thenonflower-visiting butterfly Morpho peleides (Nymphalidae) uses a sweeping technique and a brush-shaped tip to feed from surfaces.(d ) A fruit-piercing butterfly, Archaeoprepona demophoon (Nymphalidae), pushes its robust proboscis tip into fruit. (e) A piercing,occasionally blood-sucking moth, Calyptra thalictri (Noctuidae), employs antiparallel galeae movements (photo courtesy of J. Zaspel);the acute proboscis bears piercing armature. ( f ) The tear-feeding moth Lobocraspis griseifusa (Noctuidae) feeds from a buffalo’s eye(photo courtesy of W. Buttiker); the proboscis tip is equipped with rasping structures.

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Males of a notodontid moth Gluphisia septen-trionis take up large amounts of water, althoughtheir proboscis is rudimentary and they do notfeed on sugary fluids. The moth can pump anequivalent of 12% of its body mass per minutethrough the digestive tract, which amounts tomore than 600 times its body mass in 3.4 h offluid uptake (132).

Mechanism of the Sucking Pump

The functional anatomy of the sucking pumphas been studied mainly in butterflies (44, 47,50) and the hawk moth Manduca sexta (39, 108).The majority of head muscles are associatedwith the sucking pump (136), which is an ex-pandable cavity located between the proboscisand esophagus and is outfitted with valve struc-tures. Discontinuous fluid transport is achievedby coordinated and rhythmic contracting ofdilator, compressor, and sphincter muscles. Asdemonstrated in real time, X-ray imaging offeeding butterflies shows that fluid is drawn intothe pump by dorsal expansion of the cham-ber. Contraction of circular compressor mus-cles transports discrete boluses of fluid into theesophagus (133). A neuroanatomical study ofthe sucking pump in M. sexta indicates that thefrontal cibarial valve and one pair of the dilatormuscles must have originated from the cibar-ium, whereas the remaining dilator muscles,the compressor musculature, and the sphinc-ter muscle to the esophagus belong to the sto-modeum. This led to the new hypothesis thatthe sucking pump developed from the anteriorstomodeum rather than the cibarium (39). Thesucking pump muscles are innervated by thefrontal ganglion and can be triggered into ac-tion by application of a sucrose solution to theproboscis. As indicated by electrophysiologicalstudies, the dilation phase begins with contrac-tion of the esophageal sphincter and is followedby contraction of the cibarial opener muscle(39, 108). The principal composition of thesucking pump and its mechanism appears iden-tical in glossatan Lepidoptera. In nymphalidbutterflies, cibarial components form a valvethat controls the outflow of saliva into the food

canal of the proboscis during the compressionphase of the sucking pump (47).

ADAPTATIONS TO VARIOUSFOOD SOURCES

Nectar-Feeding and Flower-HandlingBehavior

Most nectar-feeding Lepidoptera are oppor-tunistic flower visitors (64) and probe flowers ofvarious sizes with open or concealed nectaries.Most descriptions of flower-handling behaviorconcern butterflies and hawk moths (44, 82, 86,125). Butterflies approach flowers with a looselycoiled proboscis and uncoil it after landing. Inthe feeding position, the proboscis shows a dis-tinct bend after approximately one third of itslength (Figure 5a), enabling the proboscis toadjust to various flower depths (7, 44, 82). Atypical sequence of probing movements con-sists of an elevation of the proboscis at the basaljoint until the tip loses contact with the sur-face, followed by extension or flexion of thebend region to move the tip of the proboscisforward or backward, and lowering of the pro-boscis until its tip again contacts the flower atanother location (Figure 5a). Butterflies oftenproduce several short series of such probingmovements lasting between 0.2 and 0.5 s andconsisting of two to five cycles (82, 86). Oncea butterfly has located the entrance to a flower,it lowers its proboscis at the base, enabling thetip to project into the flower. Depending onthe length of the proboscis and the depth ofthe flower, the proboscis is inserted up to thebend region or even further; sometimes this isaccompanied by flexion of the legs and bow-ing of the head. Brief poking movements of-ten follow in which the proboscis is partiallylifted and immediately inserted again. Duringflower probing, the sensilla styloconica presum-ably provide information on both nectar andthe position of the tip inside a flower (84). Theproboscis may remain motionless for a momentwhen nectar is ingested. When the flower is de-pleted, the proboscis is pulled out. If the butter-fly is visiting an inflorescence, it rapidly turns tothe next flower and repeats the flower-probing


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sequence. In this manner a butterfly can swiftlyprobe one flower after another by simply rotat-ing its body (86). A study of handling times inbutterflies indicates that species with a dispro-portionately long proboscis may require signifi-cantly greater length times compared to specieswith an average sized proboscis, thus amount-ing to reduced foraging efficiency (104).

Hawk moths often exploit flowers whilehovering in front of or over them; at times,the flower is grasped with the legs (125). TheSphingidae are particularly capable of extract-ing nectar from long-spurred flowers; nonethe-less, they can skillfully handle shallow flowers(2, 69, 109, 144). Stereotypical swing-hoveringflight behavior was observed in some hawkmoths (144). The tip of the proboscis is intro-duced into the corolla as far as possible wherebythe distal proboscis is often bent upward (7).Mechanosensory input is crucial for proboscisinsertion since three-dimensional features ofthe flower, such as grooves, significantly en-hance foraging performance by decreasing thetime it takes for the hawk moth to discover thenectar (66).

There is convincing evidence that the evo-lution of extremely long proboscises is associ-ated with adaptations to long-spurred flowers,in particular orchids (36, 114, 115, 128). How-ever, an alternative hypothesis argues that theevolution of the extremely long proboscis of thehawk moth Xanthopan morgani from Madagas-car could have resulted from selective pressureto escape predators, such as spiders, that lurkon flowers. Long-spurred orchids are adaptedto hawk moths, exploiting them as particularlyvaluable pollinating vectors (143, 144).

Pollen Feeding and AdditionalSources of Food

The Neotropical butterflies of the closely re-lated genera Heliconius and Laparus (Nymphal-idae) rely on pollen, in addition to floral nec-tar, as a food source (24, 51, 63). The pollengrains are actively collected on the outside ofthe proboscis during flower probing. After alump of pollen has been collected, it is agitated

in a fluid for hours by coiling and uncoil-ing movements of the proboscis (Figure 5b).The resulting liquid is ingested, but the pollengrains remain outside the body (63). Duringthis process essential amino acids are extractedfrom the pollen grains (116). Nitrogen ob-tained from amino acids benefits the produc-tion of eggs, nuptial gifts, and antipredatorysubstances, and it greatly extends life span (24,43, 63, 116). A morphologically based phy-logeny suggests that pollen feeding is conver-gent in Heliconius and Laparus (121). However,recent molecular-based phylogenies indicate asingle origin for pollen feeding with a loss inone lineage (21). The proboscises of Helico-nius butterflies are longer than those of relatednonpollen-feeding nymphalids, and they bear agreater number of long sensory bristles in theproximal half where the pollen is accumulated(90). Flower-probing movements last signifi-cantly longer on flowers when pollen is col-lected (86). Fluid exuded from the tip helpspollen stick to the proboscis and is used forpollen processing (122). The fluid, likely saliva,contains proteases that probably extract theamino acids (45). A comparative study of thesalivary glands revealed no histological differ-ences between pollen-feeding and nonpollen-feeding Heliconiinae (46). However, both thelength and the volume of salivary glands weregreater in pollen-feeding species (48).

Some species of Ithomiinae are specializedto supplement their nutrition with nitrogenfrom bird droppings. Females ingest liquidfrom fresh excrement of antbirds, which huntinsects flushed out by predatory marches ofEciton army ants (126).

In addition to floral nectar, many Lepi-doptera obtain sugar from other sources suchas extrafloral nectaries, squashed fruit, and hon-eydew, as well as mineral substances from per-spiration on human skin and from moist soil.The latter phenomenon is common to malesof many taxa and sometimes involve large ag-gregations of different species on sodden earth,dung, mammalian urine, mud puddles (1, 20,42) and, according to a single report, on marinealgae mats (124). Butterflies perform dabbing

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movements with the tip of the proboscis whenconsuming fluid from moist surfaces. Com-pared to flower probing, the uncoiled proboscisshows a less conspicuous bend region and ei-ther the tip region is directed toward the body(Figure 5c) or the proboscis is held in a nearlystraight position with the tip region flexed up-side down so that the drinking slits contact themoist surface (86).

Many adult members of the moth familyArctiidae and male Danainae and Ithomiinaebutterflies are attracted to plants that containpyrrolizidine alkaloids. They take up and in-corporate the poisonous plant substances, us-ing them as a defense against predators and, inmodified form, during courtship behavior. Thepharmacophagous butterflies discharge a fluidfrom the proboscis tip that dissolves alkaloidsfrom wilted leaves and dried parts of certainBoraginaceae and Asteraceae (26, 27).

Sweeping Technique of Feedingfrom Surfaces

A considerable number of species of the familyNymphalidae, and certain butterflies of the Ri-odinidae, Lycaenidae, and some moths of theNoctuidae, have never been observed to visitflowers (40, 41, 49, 71). Instead of nectar feed-ing, they feed on fruit, honeydew or decay-ing substances. The nonflower-visiting butter-flies of the Nymphalidae have a shorter pro-boscis than their nectar-feeding relatives. Thetip region is equipped with long, numerous,and densely ordered sensilla styloconica, whichform a flat brush (Figure 5c) that functions as astructure for accumulation of fluid (81, 92, 110).The brush-shaped tip region is interpreted tobe an adaptation to feeding on wet surfaces andpresumably evolved independently in variousphylogenetic lineages (92). Most nonflower-visiting butterflies perform a sweeping tech-nique along with dabbing movements to ingestfluid from wet surfaces of various kinds. Butter-flies of Nymphalinae and Satyrinae apply thedorsal side of the tip region to the feeding sur-face and either raise the tip and place it else-where or sweep it over the surface. Proboscis

movements differ greatly in frequency acrosssubstrates, probably depending on the textureand fluidity of the fruit (110). The butterflyMorpho peleides scans a wide area without hav-ing to move about by simply rising and loweringthe uncoiled proboscis and by sideward bendingof the particularly flexible tip region. Further, itliquefies dried fruit juice and dilutes thick juicesfor ingestion by discharging saliva (81).

Some Asian species of the family Lycaenidaefeed on honeydew produced by aphids, coc-cids, and membranicids. They also consumeextrafloral nectar, but they never visit flowers.To entice these sap-feeding insects to releasedroplets of honeydew, the butterfly taps themwith its proboscis, presumably mimicking an-tennal stimulation performed by guarding ants(60, 61).

Techniques of Fruit and Skin Piercing

Apart from surface feeding, some Lepidopterapierce their food sources to obtain the fluidinside. Nymphalid butterflies of the subfam-ily Charaxinae plunge the proboscis into softfruit, dung, or carrion (110). The butterfliessearch for injuries on the fruit through whichthey thrust their proboscises, employing move-ments of the whole body. Unlike the sweep-ing technique of fruit feeding, the proboscisis held straight, without bending (Figure 5d ).After the fruit is penetrated, the entire pro-boscis moves forward and backward without be-ing withdrawn. Fruit-piercing butterflies havehigher intake rates from soft fruit comparedwith other fruit-feeding Nymphalidae whenstandardized for body size (110). The proboscisis rather short, thick, and robust; the tip ispointed and outfitted with short sensilla stylo-conica (Figure 5d ) (92, 110).

A number of noctuid moths employ a differ-ent mechanism to pierce fruit (12, 13, 18) thatmay inflict damage to citrus crops (58). Thesemoths possess a sharp-tipped proboscis thatbears an armature of acute erectile structures,hooks, and spines (6). The erectile structuresare composed of a socket and an acute shaftcorresponding to the composition of sensilla


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styloconica, the hooks are probably homo-logues of sensilla basiconica, and the spines cor-respond to dorsal legulae of the galeal link-age (32). Banziger (6) described the elaboratetechnique, whereby even thick-walled fruit canbe pierced. It begins with a rapid vibration bywhich a small hole is drilled, and the hooksanchor the proboscis. Penetration is accom-plished by antiparallel movements of the galeae(Figure 5e), in which one and then the othergalea is pushed further into the fruit. Tiltingmovements of the head compensate for side-ward bending of the proboscis when one galeais pushed forward. The erectile structures areextended by a bulging of the cuticle due to in-creased hemolymph pressure inside the galearesulting from stipital pumping similar to theuncoiling process. The erected structures ofone galea provide resistance so that the othergalea can be pushed further into the tissue. Af-ter feeding, hemolymph pressure is decreasedinside the galeae by opening the stipes valve.The flexion of the erectile structures reversesand antiparallel movements of the galeae with-draw the proboscis.

Males of seven Asian species of Calyptra fac-ultatively pierce skin and suck blood from largemammals, including humans (6, 9, 10, 11, 15,18, 147). The proboscis armature is similar tothat in fruit-piercing moths (Figure 5e). Theproboscis tip drills a hole into the skin by tor-sion, and penetration results from antiparallelmovements of the galeae (Figure 5e). Erectilestructures provide the resistance needed to ad-vance the proboscis into the skin (10, 11). Thereis no doubt that hemophagy is derived fromfruit-piercing behavior (18).

Eye Frequenting and Tear Feeding

A considerable number of nocturnal speciesof the Pyralidae, Noctuidae, and Geometridae,and few species of the Thyatiridae, Notodonti-dae, and Sphingidae, in tropical regions of theworld regularly feed on wounds and lachrymalfluid from the eyes of large mammals, includinghumans (8, 14, 16, 17, 29, 30). These zoophilousmoths are mainly males. They approach theirhosts at night and settle near the eye to imbibelachrymal fluid (Figure 5f ).

All obligatory lachryphagous moths possessa soft proboscis tip, which is characterized byprojecting sensilla and long dentate dorsal leg-ulae, giving the tip region a serrate appearance(Figure 5f ) (29, 32). The shape of the pro-boscis and its jerky probing movements irritatethe eye (humans experience pain) and cause anincrease in lachrymal secretion (16, 17, 19). Be-cause the particular tip morphology is similar tothat in unrelated tear-feeding taxa, it is regardedas an adaptation that evolved convergently ineye-frequenting species (32). An examinationof the midgut of these moths demonstrated thepresence of leukocytes and epithelial cells (31).Proteases present in the gut of many but not alllachryphagous moths would allow for digestionof protein contents of tears (8, 18).

In contrast, the tear-feeding noctuid mothHemiceratoides hieroglyphica from Madagascarpossesses a sharp-tipped proboscis, although itfeeds from the eyes of sleeping birds. The tipis characterized by hooks and spines, similarto that in species of fruit-piercing Noctuidae(74). Details of the armature indicate a differ-ent evolutionary line than other tear-feedingLepidoptera (18).

SUMMARY POINTS

1. The evolution of the suctorial proboscis from biting-chewing mouthparts in adult Lep-idoptera is one of the best-studied examples among flower-visiting insects.

2. The evolution of the proboscis is characterized by the formation of a food tube that issealed by linking structures, by modifications of the sensory equipment, and by novel mus-culature. Each of these features can be reconstructed from the plesiomorphic conditionof the tiny galeae in biting-chewing mouthparts that have been retained in some lineages.

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3. In context with nectar feeding, the proboscis length may increase almost 100-fold; ex-tremely long proboscises evolved in the families Sphingidae, Hesperiidae, and Riodinidae.

4. A primarily hydraulic mechanism uncoils the proboscis, whereas spirally recoiling iscaused by the proboscis musculature in addition to cuticular elasticity.

5. A discontinuous flow of fluid is created by the cranial sucking pump, which allows uptakeof quantities that approximate half the body weight in a single feeding event.

6. Repeated sequences of characteristic proboscis movements permit a butterfly to swiftlyprobe flowers, in particular on inflorescences.

7. Exploitation of additional or alternative food sources often is associated with modifiedproboscis movements and derived proboscis traits that display novel functional roles inthe feeding mechanisms.

DISCLOSURE STATEMENT

The author is not aware of any affiliations, memberships, funding, or financial holdings that mightbe perceived as affecting the objectivity of this review.

ACKNOWLEDGMENT

I would like to thank Traudl Klepal and the coworkers of the Department of UltrastructureResearch and Cell Imaging (University of Vienna), Joseph Gokcezade for help with drawings,Jennifer Zaspel and the recently deceased Willi Buttiker for providing photos, as well as John Plantfor linguistic help and Barbara-Amina Gereben-Krenn for discussions. Research was supportedby the Austrian National Science Fund (P 18425-B03).

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AR397-FM ARI 12 November 2009 9:17

Annual Review ofEntomology

Volume 55, 2010Contents

FrontispieceMike W. Service � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � xiv

The Making of a Medical EntomologistMike W. Service � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 1

Ecology of Herbivorous Arthropods in Urban LandscapesMichael J. Raupp, Paula M. Shrewsbury, and Daniel A. Herms � � � � � � � � � � � � � � � � � � � � � � � � � �19

Causes and Consequences of Cannibalism in Noncarnivorous InsectsMatthew L. Richardson, Robert F. Mitchell, Peter F. Reagel,and Lawrence M. Hanks � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �39

Insect Biodiversity and Conservation in AustralasiaPeter S. Cranston � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �55

Ekbom Syndrome: The Challenge of “Invisible Bug” InfestationsNancy C. Hinkle � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �77

Update on Powassan Virus: Emergence of a North AmericanTick-Borne FlavivirusGregory D. Ebel � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � �95

Beyond Drosophila: RNAi In Vivo and Functional Genomics in InsectsXavier Belles � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 111

DicistrovirusesBryony C. Bonning and W. Allen Miller � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 129

Olive Fruit Fly: Managing an Ancient Pest in Modern TimesKent M. Daane and Marshall W. Johnson � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 151

Insect Silk: One Name, Many MaterialsTara D. Sutherland, James H. Young, Sarah Weisman, Cheryl Y. Hayashi,and David J. Merritt � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 171

Bayesian Phylogenetics and Its Influence on Insect SystematicsFredrik Ronquist and Andrew R. Deans � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 189

Insect Fat Body: Energy, Metabolism, and RegulationEstela L. Arrese and Jose L. Soulages � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 207

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Sex Differences in Phenotypic Plasticity Affect Variation in Sexual SizeDimorphism in Insects: From Physiology to EvolutionR. Craig Stillwell, Wolf U. Blanckenhorn, Tiit Teder, Goggy Davidowitz,Charles W. Fox � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 227

Facultative Symbionts in Aphids and the Horizontal Transfer ofEcologically Important TraitsKerry M. Oliver, Patrick H. Degnan, Gaelen R. Burke, and Nancy A. Moran � � � � � � � � � 247

Honey Bees as a Model for Vision, Perception, and CognitionMandyam V. Srinivasan � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 267

Invasion Biology, Ecology, and Management of the Light Brown AppleMoth (Tortricidae)D.M. Suckling and E.G. Brockerhoff � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 285

Feeding Mechanisms of Adult Lepidoptera: Structure, Function, andEvolution of the MouthpartsHarald W. Krenn � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 307

Integrated Management of Sugarcane Whitegrubs in Australia:An Evolving SuccessPeter G. Allsopp � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 329

The Developmental, Molecular, and Transport Biology of MalpighianTubulesKlaus W. Beyenbach, Helen Skaer, and Julian A.T. Dow � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 351

Biorational Approaches to Managing Stored-Product InsectsThomas W. Phillips and James E. Throne � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 375

Parallel Olfactory Systems in Insects: Anatomy and FunctionC. Giovanni Galizia and Wolfgang Rossler � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 399

Integrative Taxonomy: A Multisource Approach to ExploringBiodiversityBirgit C. Schlick-Steiner, Florian M. Steiner, Bernhard Seifert,Christian Stauffer, Erhard Christian, and Ross H. Crozier � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 421

Evolution of Plant Defenses in Nonindigenous EnvironmentsColin M. Orians and David Ward � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 439

Landscape Epidemiology of Vector-Borne DiseasesWilliam K. Reisen � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 461

Role of Adhesion in Arthropod Immune RecognitionOtto Schmidt, Kenneth Soderhall, Ulrich Theopold, and Ingrid Faye � � � � � � � � � � � � � � � � � � � � 485

Physical Ecology of Fluid Flow Sensing in ArthropodsJerome Casas and Olivier Dangles � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 505

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Managing Invasive Populations of Asian Longhorned Beetle and CitrusLonghorned Beetle: A Worldwide PerspectiveRobert A. Haack, Franck Herard, Jianghua Sun, and Jean J. Turgeon � � � � � � � � � � � � � � � � � 521

Threats Posed to Rare or Endangered Insects by Invasions ofNonnative SpeciesDavid L. Wagner and Roy G. Van Driesche � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 547

Malaria Management: Past, Present, and FutureA. Enayati and J. Hemingway � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 569

Regulation of Midgut Growth, Development, and MetamorphosisRaziel S. Hakim, Kate Baldwin, and Guy Smagghe � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 593

Cellulolytic Systems in InsectsHirofumi Watanabe and Gaku Tokuda � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 609

Indexes

Cumulative Index of Contributing Authors, Volumes 46–55 � � � � � � � � � � � � � � � � � � � � � � � � � � � 633

Cumulative Index of Chapter Titles, Volumes 46–55 � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � � 638

Errata

An online log of corrections to Annual Review of Entomology articles may be found athttp://ento.annualreviews.org/errata.shtml

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Feeding Mechanisms of Adult Lepidoptera: Structure...

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