One proboscis, two tasks: Adaptations to blood-feeding and nectar-extracting in long-proboscid horse flies (Tabanidae, Philoliche)

Karolyi, Florian; Colville, Jonathan F.; Handschuh, Stephan; Metscher, Brian; Krenn, Harald W.

doi:10.1016/j.asd.2014.07.003

Cited by 42 publications

(31 citation statements)

References 45 publications

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“…There has an emphasis in investigating the drinking patterns of animals that use tongues or tongue-like devices to load fluid (Karolyi et al 2014;Krenn 2010;Kingsolver and Daniel 1983;Winter and von Helversen 2003). Most tongues and tongue-like devices are considered just as rigid bodies with permanent surfaces during drinking process, such as the tongues of butterflies , shorebirds (Prakash et al 2008), cats (Reis et al 2010) and dogs (Crompton and Musinsky 2011).…”

Section: Introductionmentioning

confidence: 99%

Feeding Kinematics and Nectar Intake of the Honey Bee Tongue

Zhu

Liu

et al. 2016

J Insect Behav

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Most flower-visiting insects employ highly-evolved organs to feed themselves rapidly and efficiently on the floral nectar. A honey bee drives its segmented tongue (glossa) covered by dense hairs reciprocatingly to load nectar. A high-speed camera system ameliorated by a microscope revealed morphological changes in glossal surfaces during live honey bees' nectar dipping and surface configurations through the stretching of postmortem honey bees' glossae. Both the in vivo and postmortem observations reveal that shortening and lengthening of the glossal segments perform high concordance with the erection of glossal hairs, which aids in developing deformable gaps between rows of glossal hairs during nectar trapping. A model was proposed to evaluate the nectar-intake volume considering the experimentally-measured average erection angle and tongue elongation length during nectar feeding. The theoretical results fit the experimental data well and disclose that these two factors contribute to an augmentation of nectar-intake observably. We also theoretically present that the extendible and deformable glossae have advantages for the polylectic feeding behavior.

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Section: Introductionmentioning

confidence: 99%

Feeding Kinematics and Nectar Intake of the Honey Bee Tongue

Zhu

Liu

et al. 2016

J Insect Behav

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“…Most conspicuous are elongations of the mouthparts which are often shaped as a proboscis in insects (Krenn et al ., ). Euglossine bees, certain tabanid and nemestrinid flies and some hawk moths have evolved extremely long mouthparts that exceed twice the body length to gain access to long‐tubed flowers (Amsel, ; Borrell, ; Borrell & Krenn, ; Pauw et al ., ; Karolyi et al ., , ). However, such extremely long mouthparts are rare among butterflies.…”

Section: Introductionmentioning

confidence: 99%

Functional constraints on the evolution of long butterfly proboscides: lessons from Neotropical skippers (Lepidoptera: Hesperiidae)

Bauder

Morawetz

Warren

et al. 2015

J of Evolutionary Biology

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Extremely long proboscides are rare among butterflies outside of the Hesperiidae, yet representatives of several genera of skipper butterflies possess proboscides longer than 50 mm. Although extremely elongated mouthparts can be regarded as advantageous adaptations to gain access to nectar in deep-tubed flowers, the scarcity of long-proboscid butterflies is a phenomenon that has not been adequately accounted for. So far, the scarceness was explained by functional costs arising from increased flower handling times caused by decelerated nectar intake rates. However, insects can compensate for the negative influence of a long proboscis through changes in the morphological configuration of the feeding apparatus. Here, we measured nectar intake rates in 34 species representing 21 Hesperiidae genera from a Costa Rican lowland rainforest area to explore the impact of proboscis length, cross-sectional area of the food canal and body size on intake rate. Long-proboscid skippers did not suffer from reduced intake rates due to their large body size and enlarged food canals. In addition, video analyses of the flower-visiting behaviour revealed that suction times increased with proboscis length, suggesting that long-proboscid skippers drink a larger amount of nectar from deep-tubed flowers. Despite these advantages, we showed that functional costs of exaggerated mouthparts exist in terms of longer manipulation times per flower. Finally, we discuss the significance of scaling relationships on the foraging efficiency of butterflies and why some skipper taxa, in particular, have evolved extremely long proboscides.

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“…The probes of these insects allow the delivery of eggs or fluids, such as venom, and/or the withdrawal of fluids, such as phloem sap and blood. Butterflies and flies that probe in solid substrates generally have rather short and stiff probes, with limited insertion depth (Krenn, 2010;Karolyi et al, 2014). The presence of musculature inside the probe in butterflies (Krenn, 2010) presumably limits the length/width ratio (l/w), also called slenderness.…”

Section: Introductionmentioning

confidence: 99%

Functional principles of steerable multi‐element probes in insects

et al. 2018

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Hemipterans, mosquitoes, and parasitic wasps probe in a variety of substrates to find hosts for their larvae or food sources. Probes capable of sensing and precise steering enable insects to navigate through solid substrates without visual information and to reach targets that are hidden deep inside the substrate. The probes belong to non‐related taxa and originate from abdominal structures (wasps) or mouthparts (hemipterans and mosquitoes), but nevertheless share several morphological characteristics. Although the transport function clearly differs (egg laying and acquisition of liquid food), the functional demands on the mechanical behaviour of the probe within the substrate tend to be similar. The probe needs to be thin to limit substrate deformation, and long, in order to attain substantial path lengths or depths. We linked the morphology across taxa to the different functional requirements, to provide insights into the biology of probing insects and the evolution of their probes. Current knowledge of insect probes is spread over many taxa, which offers the possibility to derive general characteristics of insect probing. Buckling during initial puncturing is limited by external support mechanisms. The probe itself consist of multiple (3–6) parts capable of sliding along one another. This multi‐part construction presumably enables advancement and precise three‐dimensional steering of the probe through the substrate with very low net external pushing forces, preventing buckling during substrate penetration. From a mechanical viewpoint, a minimum of three elements is required for 3D steering and volumetric exploration, as realised in the ovipositors of wasps. More elements, such as in six‐element probes of mosquitoes, may enhance friction in soft substrates. Alternatively, additional elements can have functions other than ‘drilling’, such as saliva injection in mosquitoes. Despite the gross similarities, probes show differences in their cross sections, tip morphologies, relative lengths of their elements, and the shape of their interconnections. The hypothesis is that the probe morphology is influenced by the substrate properties, which are mostly unknown. Correlating the observed diversity to substrate‐specific functional demands is therefore currently impossible. We conclude that a multipart probe with sliding elements is highly effective for volumetric substrate probing. Shared functional demands have led to an evolutionary convergence of slender multi‐element probes in disparate insect taxa. To fully understand 3D probing, it is necessary to study the sensory and material properties, as well as the detailed kinematics and dynamics of the various probes in relation to the nature of the selective pressure originating from the species‐specific substrates. Such knowledge will deepen our understanding of probing mechanisms and may support the development of slender, bio‐inspired probes.

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One proboscis, two tasks: Adaptations to blood-feeding and nectar-extracting in long-proboscid horse flies (Tabanidae, Philoliche)

Cited by 42 publications

References 45 publications

Feeding Kinematics and Nectar Intake of the Honey Bee Tongue

Feeding Kinematics and Nectar Intake of the Honey Bee Tongue

Functional constraints on the evolution of long butterfly proboscides: lessons from Neotropical skippers (Lepidoptera: Hesperiidae)

Functional principles of steerable multi‐element probes in insects

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