Feeding mechanisms of adult Lepidoptera: structure, function, and evolution of the mouthparts

Abstract

The form and function of the mouthparts in adult Lepidoptera and their feeding behavior are reviewed from evolutionary and ecological points of view. The formation of the suctorial proboscis encompasses a fluid-tight food tube, special linking structures, modified sensory equipment, and novel intrinsic musculature. The evolution of these functionally important traits can be reconstructed within the Lepidoptera. The proboscis movements are explained by a hydraulic mechanism for uncoiling, whereas recoiling is governed by the intrinsic proboscis musculature 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 handling. Behavioral modifications and derived proboscis morphology are often associated with specialized feeding preferences or an obligatory switch to alternative food sources.

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.

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).

Figure 3

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

Figure 4

Functional mechanisms of the proboscis movements in Lepidoptera. Schematic illustration of a lateral view of 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 tubular part 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) and proboscis elasticity; contraction of internal stipes muscle (ism) flexes the proboscis into the resting position.

Figure 5

Examples of Lepidoptera feeding on various food sources (arrows indicate proboscis movements) and corresponding characteristic proboscis morphology (scanning electron micrographs). (a) A nectar-feeding butterfly, Argynnis paphia (Nymphalidae), possesses a slender proboscis tip. (b) A pollen-feeding butterfly, Heliconius pachinus (Nymphalidae), with a load of pollen on the proboscis. (c) The nonflower-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.