Harald W. Krenn

Feeding Mechanisms of Adult Lepidoptera: Structure, Function, and Evolution of the Mouthparts

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.

Functional morphology and movements of the proboscis of Lepidoptera (Insecta)

SummaryThe mouthparts of Lepidoptera were investigated in a number of species by morphological and cinematographical methods. Both the galeae (which compose the proboscis) and the basal maxillary components (stipites) were studied in the resting position, in motion, and during feeding. In the resting position the proboscis is coiled so tightly that the surfaces of the consecutive coils are in close contact and the outermost coil touches the ventral side of the head. Cuticular processes of the galeal wall interlock between the coils in this position. In the investigated species they occur on the galeal wall and on the ventral side of the head in varying number and distribution. By the extension of the basal galeal joint, the coiled proboscis is released from its resting position and is elevated continuously. It uncoils in 3–5 steps which effect the entire length simultaneously. Each uncoiling step occurs synchronously with a compression of the stipital tubes on either side of the body. These compression movements pump hemolymph into the galeae. In all investigated Lepidoptera the uncoiled proboscis shows a distinct downward bend at a certain point which is also detectable in anaesthetized or freshly killed animals in some species. This feeding position and the movements of the uncoiled proboscis are similar in all species despite the intrinsic galeal muscles being variously arranged in the galeal lumen in different Lepidoptera. When comparing cross-sections through corresponding regions of coiled and uncoiled proboscises, the curvatures of the dorsal galeal walls remain unchanged. Coiling of the proboscis starts at the tip and progresses to the base. After coiling the proboscis tightly beneath the head, the diameter of the spiral widens due to its elastic properties until the proboscis props itself against the ventral side of the head. This elastic effect combined with the interlocking cuticular processes seems to be responsible for the resting position of the proboscis.

Origin of a complex key innovation in an obligate insect-plant mutualism.

Evolutionary key innovations give organisms access to new ecological resources and cause rapid, sometimes spectacular adaptive radiation. The well known obligate pollination mutualism between yuccas and yucca moths is a major model system for studies of coevolution, and it relies on the key innovation in the moths of complex tentacles used for pollen collecting and active pollination. These structures lack apparent homology in other insects, making them a rare example of a novel limb. We performed anatomical and behavioral studies to determine their origin and found evidence of a remarkably simple mechanism. Morphological analyses of the tentacles and adjacent mouthparts in pollinators and closely related taxa showed that the tentacle appears abruptly in female pollinating yucca moths. Several morphological synapomorphies between the galeae, which constitute the characteristic lepidopteran proboscis, and the tentacle suggest that the tentacle evolved quickly through expression of the genetic template for the galea at an apical growth bud on the first segment of the maxillary palp. Behavioral data indicate that tentacle and proboscis movements are controlled by a shared hydraulic extension mechanism, thus no new mechanism was needed for tentacle function. Known developmental paths from other insects can explain the origin of this sex-specific key innovation in a few steps.

Mouthparts of heliconius butterflies (LEPIDOPTERA : NYMPHALIDAE) : a search for anatomical adaptations to pollen-feeding behavior

Abstract Proboscis length, the length of the tip, the number and length of the various sensilla throughout the proboscis, and the size and shape of the labial palpi were compared in 25 species of pollen-feeding and non-pollen-feeding Heliconiinae (Lepidoptera, Nymphalidae). The mouthparts of pollen-feeding species (all belonging to the genera Heliconius and Laparus ) do not have structures exclusive to them. However, in comparison with non-pollen-feeding Heliconiiti, the pollen-feeding species have a significantly longer proboscis without elongation of the tip-region ; the bristle-shaped sensilla trichodea were found to be significantly more numerous and longer on the proximal and mid-region of the proboscis, while the sensilla of the tip-region are significantly shorter. In addition to these proboscis features, the labial palpi were shorter in the pollen-feeding species, which is likewise possibly associated with pollen-feeding behavior. The biological role of these features is discussed and the evolution of this unique feeding behavior among Lepidoptera is considered in the context of the phylogenetic relationships among genera of Heliconiini.

Proboscis sensilla in Vanessa cardui (Nymphalidae, Lepidoptera): functional morphology and significance in flower-probing

Abstract Morphology and distribution of the proboscis sensilla in Vanessa cardui have been investigated in order to contribute to the understanding of flower-probing behaviour in butterflies. The proboscis has a bend region approximately one-third of the length from the base. A short tip region is characterized by rows of intake slits leading into the food canal. Along the dorsal, lateral and ventral sides of the proboscis, sensilla trichodea, sensilla basiconica and sensilla styloconica are distributed in varying patterns depending on their distance from the b ase. The medial food canal bears one longitudinal row of sensilla basiconica only. The bristle-shaped sensilla trichodea are longer in the proximal region of the proboscis and become gradually shorter towards the tip. They are most frequent in number near to the bend region and near the beginning of the tip region. Sensilla basiconica arranged in longitudinal rows increase in number the more distal they are on the proboscis. The tip region is characterized by rows of sensilla styloconica on the dorsal side whereas the sensilla trichodea are mostly restricted to the ventral side. The ultrastructure suggests that the aporous sensilla trichodea function as mechanosensilla while the uniporous sensilla basiconica act as contact chemosensilla. The sensilla styloconica are regarded as bimodal contact chemo/mechanosensilla since their sensory cones are equipped with a single terminal pore and a tubular body at the base. The mouthpart sensilla appear to provide tactile cues on the positioning of the proboscis and on the degree of its insertion into a floral tube. Furthermore, they receive chemical stimuli on the availability of nectar and on the immersion status of the food canal.

Hard times in the city - attractive nest sites but insufficient food supply lead to low reproduction rates in a bird of prey.

IntroductionUrbanization is a global phenomenon that is encroaching on natural habitats and decreasing biodiversity, although it is creating new habitats for some species. The Eurasian kestrel (Falco tinnunculus) is frequently associated with urbanized landscapes but it is unclear what lies behind the high densities of kestrels in the urban environment.ResultsOccupied nest sites in the city of Vienna, Austria were investigated along a gradient of urbanization (percentage of land covered by buildings or used by traffic). Field surveys determined the abundance of potential prey (birds and rodents) and the results were compared to the birds’ diets. A number of breeding parameters were recorded over the course of three years. The majority of kestrels breed in semi-natural cavities in historic buildings. Nearest neighbour distances (NND) were smallest and reproductive success lowest in the city centre. Abundance of potential prey was not found to relate to the degree of urbanization but there was a significant shift in the birds’ diets from a heavy reliance on rodents in the outskirts of the city to feeding more on small birds in the centre. The use of urban habitats was associated with higher nest failure, partly associated with predation and nest desertion, and with significantly lower hatching rates and smaller fledged broods.ConclusionsHigh breeding densities in urban habitats do not necessarily correlate with high habitat quality. The high density of kestrel nests in the city centre is probably due to the ready availability of breeding cavities. Highly urbanized areas in Vienna are associated with unexpected costs for the city dwelling-raptor, in terms both of prey availability and of reproductive success. The kestrel appears to be exploiting the urban environment but given the poor reproductive performance of urban kestrels it is likely that the species is falling into an ecological trap.

Form, function and evolution of the mouthparts of blood-feeding Arthropoda☆

This review compares the mouthparts and their modes of operation in blood-feeding Arthropoda which have medical relevance to humans. All possess piercing blood-sucking proboscides which exhibit thin stylet-shaped structures to puncture the hosts skin. The tips of the piercing structures are serrated to provide anchorage. Usually, the piercing organs are enveloped by a soft sheath-like part which is not inserted. The piercing process includes either back and forth movements of the piercing structures, or sideways cutting motions, or the apex of the proboscis bears teeth-like structures which execute drilling movements. Most piercing-proboscides have a food-canal which is separate from a salivary canal. The food-canal is functionally connected to a suction pump in the head that transports blood into the alimentary tract. The salivary canal conducts saliva to the tip of the proboscis, from where it is discharged into the host. Piercing blood-sucking proboscides evolved either from (1) generalized biting-chewing mouthparts, (2) from piercing mouthparts of predators, or plant sap or seed feeders, (3) from lapping or sponging mouthparts. Representatives of one taxon of Acari liquefy skin tissue by enzymatic action. During feeding, many blood-feeding arthropods inadvertently transmit pathogens, which mostly are transported through the discharged saliva into the host.

The proboscis of eye-frequenting and piercing Lepidoptera (Insecta)

The external structures of the proboscis are investigated in eye-frequenting species of Noctuidae, Geometridae and Pyralidae by means of scanning electron microscopy. They are compared with non-eye-frequenting representatives of these families. In Noctuidae, highly specialized fruit-piercing, skin-piercing blood-sucking, and sweat-feeding representatives have been included. All hemi- and eulachryphagous species have a soft proboscis tip which is characterized by few sensilla and strongly elongated, dentate plates of the dorsal galeal linkage. The latter structures leave broad gaps between them that lead into the food canal at the tip. This arrangement permits the uptake of fluid suspensions such as lachrymal fluid, wound exudates and pus. The modified dorsal galeal linkage is regarded as an adaptation for this highly derived feeding habit. The rough surface of the proboscis is likely to cause irritation and possible mechanical damage to the conjunctiva and cornea which results in an increased lachrymal flow and production of pus. In contrast to fruit-piercing and skin-piercing Noctuidae, there are no erectile structures on the proboscis of eye-frequenting species.—The comparison with related non-eye-frequenting species demonstrates that the particular morphology of the proboscis tip in lachryphagous moths evolved convergently in different families of Leipdoptera.

Efficiency of Fruit Juice Feeding in Morpho peleides (Nymphalidae, Lepidoptera)

We have described the feeding behavior of the frugivorous butterfly Morpho peleides (Butler 1872) under various conditions and tested its ability to take up fluid from selected natural and artificial food sources in comparison with the nectarvorous Vanessa cardui (Linnaeus 1758). Both nymphalids showed similar probing behavior except for one particular proboscis movement and the fact that M. peleides was unable to feed from Lantana flowers. In 2-min feeding trials, M. peleides imbibed a greater amount of fluid from the food sources, with the most conspicuous difference on rotting banana. Without time restriction, M. peleides gained a significantly greater percentage of body weight from soaked plotting paper, whereas nosignificant difference occurred from tubular artificial flowers. The ability of M. peleides to feed more efficiently from wet surfaces than V. cardui is discussed in context with proboscis morphology.

Morphology and function of the proboscis in Bombyliidae (Diptera, Brachycera) and implications for proboscis evolution in Brachycera.

Abstract Based on serial semithin sections and SEM photographs of representatives of European Bombyliinae and Anthracinae, the mouthparts of Bombyliidae are studied and compared with the relevant data from literature on other families of Diptera Brachycera. The three moving units of the proboscis (clypeo-cibarial region, haustellum-maxillary base region, and labella) and their structures and muscles are described. Functions and possible movements are inferred from the structures observed. Articulations both between the parts of the organ and to the head capsule enable the fly to retract its proboscis into a resting position. Proboscis movement from a resting to a feeding position encompasses the following submovements: rotating of the basal clypeo-cibarial region (= fulcrum) against the head capsule, folding of the haustellum-maxillary base region against the fulcrum, evagination and invagination of the labial base, and the labella movements. This is a novelty as compared to the rigid proboscis of Tabanidae and agrees largely with the conditions in the Cyclorrhapha. The evolution of these novelties and their functional significance are discussed. The fulcrum, as well as the haustellum-maxillary base, as the new moving units are deduced from the plesiomorphic state as present in Tabanidae by fusions of sclerites, shifts of musculature and formation of new articulations.