ANRV397-EN55-17 ARI 2 November 2009 12:12 Feeding Mechanisms of Adult Lepidoptera: Structure, Function, and Evolution of the Mouthparts Harald W. Krenn Department of Evolutionary Biology, University of Vienna, A 1090 Vienna, Austria; email: [email protected] Annu. Rev. Entomol. 2010. 55:307–27 Key Words The Annual Review of Entomology is online at proboscis, fluid uptake, flower visiting, feeding behavior, insects ento.annualreviews.org This article’s doi: Abstract 10.1146/annurev-ento-112408-085338 The form and function of the mouthparts in adult Lepidoptera and Copyright c 2010 by Annual Reviews. their feeding behavior are reviewed from evolutionary and ecological All rights reserved points of view. The formation of the suctorial proboscis encompasses a 0066-4170/10/0107-0307$20.00 fluid-tight food tube, special linking structures, modified sensory equip- Annu. Rev. Entomol. 2010.55:307-327. Downloaded from arjournals.annualreviews.org by University of Vienna - Central Library for Physics on 12/07/09. For personal use only. ment, and novel intrinsic musculature. The evolution of these function- ally important traits can be reconstructed within the Lepidoptera. The proboscis 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 by the action of the cranial sucking pump, which enables uptake of a wide range of fluid quantities from different food sources. Nectar-feeding species exhibit stereotypical proboscis movements during flower han- dling. Behavioral modifications and derived proboscis morphology are often associated with specialized feeding preferences or an obligatory switch to alternative food sources. 307 ANRV397-EN55-17 ARI 2 November 2009 12:12 INTRODUCTION comprehensively in a phylogenetic context (96, 98, 103). Here, I focus on the evolution of func- The Lepidoptera (butterflies and moths) are tionally important traits of the proboscis, the Plesiomorphic: one of the most diverse taxa of animals contain- mechanisms of proboscis movements and fluid character of ancestral ing about 160,000 described species in 47 su- uptake, as well as feeding behavior on flowers condition, present perfamilies (103). Both the larval and the adult before the last and adaptations to other food sources. stages of nearly all species are associated with common ancestor of the taxon vascular plants. Most larvae feed on plant mate- rial using biting-chewing mouthparts. The ma- COMPOSITION AND jority of adults are anthophilous; they possess EVOLUTION OF LEPIDOPTERAN a proboscis that is used to imbibe floral nec- MOUTHPARTS tar and other liquid substances. The role of Lepidoptera as pollinators has been demon- Biting-Chewing Mouthparts strated in many cases of mutualistic relation- in Adult Lepidoptera ships with flowers and floral specialization (59, The origin of the lepidopteran proboscis can 79, 113, 125, 128). Their adaptation to flower be traced back to the pair of small galeae morphology provided classical examples of re- of uncertain function in the plesiomorphic ciprocal adaptations in insect-flower interac- biting-chewing mouthparts retained in non- tions (36). After Charles Darwin examined the glossatan moths of the families Micropterigidae flower of a star orchid possessing an approxi- (Figure 1), Agathiphagidae, and Heterobath- mately 300-mm-long nectar spur, he predicted miidae (54, 72, 87, 95, 98, 140). the existence of a hawk moth with a proboscis of The Micropterigidae possess a complete set matching length (36) that was actually discov- of mouthpart structures that are well adapted ered 40 years later (114). The fossil record of for collecting and grinding angiosperm pollen Lepidoptera dates back to the Jurassic period, or fern spores (33, 72, 97, 140). Covered by the yet the evolution of present-day species-rich labrum, the asymmetrical mandibles act like a lineages are probably related to the radiation mortar and pestle to crush pollen grains. The of angiosperms during the Cretaceous within maxilla consisting of cardo and stipes gives rise a relatively short time frame (145). The shift to the small lacinia on the median side, as well of larval feeding to angiosperm foliage could as the short galea and the large, five-segmented have been crucially linked with the evolution of maxillary palp (Figure 1a). The galea is adult nectar feeding and the adaptive radiation equipped with microtrichia, a row of lamellate of glossatan Lepidoptera (136). setae, few uniporous sensilla, and bristle-shaped The mouthparts of Lepidoptera belong to sensilla, as well as one small muscle attached to one of the best-studied feeding organs of the stipes (33, 53, 72, 88). The maxillary palp flower-visiting insects, in terms of anatomy, scrapes pollen out of anthers (72). Pollen grains Annu. Rev. Entomol. 2010.55:307-327. Downloaded from arjournals.annualreviews.org functional morphology, and evolutionary bi- adhere to the paddle- and mushroom-shaped by University of Vienna - Central Library for Physics on 12/07/09. For personal use only. ology (91). Several benchmark morphological bristles of the apical segment (Figure 1b), studies, dating from the latter half of the twen- which transport the pollen to the mandibles tieth century, led to the establishment of a phy- (33, 53). The labium bears a pair of short logenetic classification of the major lineages two-segmented labial palps, which bear apical of Lepidoptera that was strongly supported sensory pit organs (33). Species of Micropterix by arguments regarding mouthpart structures feed on a variety of flowers (97), whereas (38, 95, 101, 112). This high-level classifica- those of Sabatinca usually feed on pollen of tion, based on morphology, has remained ro- Zygogynum (Winteraceae) flowers, which are bust in light of present-day molecular-based pollinated during the search for pollen (138). phylogenies (62, 146). The anatomy of the These moths use paddle- and spatula-shaped lepidopteran mouthparts has been reviewed sensilla for pollen collecting (55). Whether 308 Krenn ANRV397-EN55-17 ARI 2 November 2009 12:12 a b lrlr mpmp mpmp gaga lrlr gaga lplp 100100 µmµm 5050 µmµm Figure 1 Head of Micropterix aruncella (Micropterigidae) (scanning electron micrographs) illustrating the plesiomorphic biting-chewing condition of mouthparts in adult Lepidoptera. (a) The labrum (lr) covers the mandibles. The maxilla bears the galea (ga) and the five-segmented maxillary palp (mp). The labium bears a pair of two-segmented labial palps (lp). (b) Concave short galea (ga); apical segment 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- of all major constituents of the mouthparts, ex- certain; nonetheless, their mandibles are used cept the galeae and the labial palps (136). The to open the pupal casing for emergence (97). other components of the mouthparts play no Adult Heterobathmiidae frequent flowers of role in food uptake but may have sensory func- Nothofagus (Nothofagaceae) to feed on pollen; tion during foraging. in addition, they have been observed to drink In species with a functional proboscis, the water (102). Their mouthparts are similar to labrum forms a small plate over the basal pro- those of the Micropterigidae (99) and are well boscis joint, where bristles of the pilifers con- adapted to collect and grind pollen, but only tact the basal galeal joint; these sensory bristles one type of so-called prehensile sensilla occurs probably detect proboscis movements (53, 84, on the maxillary palp, where pollen and fern 87). The mandibles are reduced and nonfunc- spores are frequently found (54). tional. The basal maxillary sclerites—the stipes and the cardo—form a tubular component from Autapomorphy: which the coilable galea and the maxillary palp derived character, Annu. Rev. Entomol. 2010.55:307-327. Downloaded from arjournals.annualreviews.org by University of Vienna - Central Library for Physics on 12/07/09. For personal use only. Mouthparts of Glossata and Evolution unique to a taxon emerge (Figure 2b); a lacinia is absent (98). of the Proboscis The maxillary palps are composed of five Glossata: taxon of Lepidoptera The great majority of adult Glossata possess segments in the plesiomorphic condition, comprising more than a coilable proboscis (Figure 2), which evolved but are short and reduced in the number of 99% of species; only once, thus representing an autapomorphy segments in most species of Ditrysia (98). The characterized by the of this clade. Adult Glossata take up only liquid biological role of the maxillary palps remains coilable proboscis, food and achieve this exclusively by way of the unclear despite the presence of sensilla in var- among other traits food tube of the proboscis, which is composed ious lineages (52, 53, 57). In the females of the Ditrysia: taxon of Lepidoptera of the medially concave and interlocked galeae. yucca moth, Tegeticula and Parategeticula (Pro- characterized by The origin of the proboscis and the transition to doxidae), the second segment of the maxillary specialized female feeding on liquids resulted in the reinforcement palpus is extended into a long coilable tentacle genital apparatus of the sucking pump in the head and a reduction that is used to collect pollen and to actively www.annualreviews.org • Feeding Mechanisms of Adult Lepidoptera 309 ANRV397-EN55-17 ARI 2 November 2009 12:12 a b pipi mpmp gaga llpp stst c p sstsst dldl 500500 µmµm 101 0 µmµm 100100 µmµm Figure 2 Head of the butterfly Vanessa cardui (Nymphalidae) (scanning electron micrographs). (a) The proboscis (p) is coiled in the resting position; 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 is characterized by sensilla styloconica (sst) and slits between the dorsal linking structures (dl).