Lepidopteran mouthpart architecture suggests a new mechanism of fluid uptake by insects with long proboscises (original) (raw)
Related papers
Zoologischer Anzeiger - A Journal of Comparative Zoology, 2005
The food canal of the proboscis of Lepidoptera serves for the uptake of nutrient fluids and the discharge of saliva. A valve was discovered at the entrance to the sucking pump in the head that separates these countercurrent flows in nymphalid butterflies. Three species of Nymphalidae were examined by dissections and light microscopic serial semithin sections. The sucking pump is a unit composed of three structures: (1) the oral valve, which is a projection of the epipharynx extending into the anterior cibarial lumen, (2) the expandable lumen, and (3) the posterior sphincter valve which controls influx into the oesophagus. Based on the microanatomical results, a functional model is presented to account for the uptake and swallowing of fluids and for the control of the salivary flow into the food canal of the proboscis. Dilator muscles of the sucking pump expand the lumen by pulling on the muscular dorso-anterior side. This opens the oral valve and fluid can be drawn into the lumen from the food canal of the proboscis. Circular compressor muscles which attach to both sides of the sclerotized ventro-posterior wall of the sucking pump reduce the size of the lumen; passively they close the oral valve and press fluid through the relaxed posterior sphincter opening into the oesophagus. According to this model saliva can be discharged into the food canal during the swallowing phase. The oral valve and pumping unit are similar in all studied species despite the fact that saliva presumably plays a special role in the derived pollen-feeding behaviour of one of them, viz. Heliconius melpomene.
Paradox of the drinking-straw model of the butterfly proboscis
The Journal of experimental biology, 2014
Fluid-feeding Lepidoptera use an elongated proboscis, conventionally modeled as a drinking straw, to feed from pools and films of liquid. Using the monarch butterfly, Danaus plexippus (Linnaeus), we show that the inherent structural features of the lepidopteran proboscis contradict the basic assumptions of the drinking-straw model. By experimentally characterizing permeability and flow in the proboscis, we show that tapering of the food canal in the drinking region increases resistance, significantly hindering the flow of fluid. The calculated pressure differential required for a suction pump to support flow along the entire proboscis is greater than 1 atm (~101 kPa) when the butterfly feeds from a pool of liquid. We suggest that behavioral strategies employed by butterflies and moths can resolve this paradoxical pressure anomaly. Butterflies can alter the taper, the interlegular spacing and the terminal opening of the food canal, thereby controlling fluid entry and flow, by splayin...
Mouthpart conduit sizes of fluid-feeding insects determine the ability to feed from pores
Proceedings. Biological sciences, 2017
Fluid-feeding insects, such as butterflies, moths and flies (20% of all animal species), are faced with the common selection pressure of having to remove and feed on trace amounts of fluids from porous surfaces. Insects able to acquire fluids that are confined to pores during drought conditions would have an adaptive advantage and increased fitness over other individuals. Here, we performed feeding trials using solutions with magnetic nanoparticles to show that butterflies and flies have mouthparts adapted to pull liquids from porous surfaces using capillary action as the governing principle. In addition, the ability to feed on the liquids collected from pores depends on a relationship between the diameter of the mouthpart conduits and substrate pore size diameter; insects with mouthpart conduit diameters larger than the pores cannot successfully feed, thus there is a limiting substrate pore size from which each species can acquire liquids for fluid uptake. Given that natural select...
Mouthpart separation does not impede butterfly feeding
Arthropod Structure & Development, 2014
The functionality of butterfly mouthparts (proboscis) plays an important role in pollination systems, which is driven by the reward of nectar. Proboscis functionality has been assumed to require action of the sucking pump in the butterfly's head coupled with the straw-like structure. Proper proboscis functionality, however, also is dependent on capillarity and wettability dynamics that facilitate acquisition of liquid films from porous substrates. Due to the importance of wettability dynamics in proboscis functionality, we hypothesized that proboscides of eastern black swallowtail (Papilio polyxenes asterius Stoll) (Papilionidae) and cabbage butterflies (Pieris rapae Linnaeus) (Pieridae) that were experimentally split (i.e., proboscides no longer resembling a sealed straw-like tube) would retain the ability to feed. Proboscides were split either in the drinking region (distal 6e10% of proboscis length) or approximately 50% of the proboscis length 24 h before feeding trials when butterflies were fed a red food-coloring solution. Approximately 67% of the butterflies with proboscides split reassembled prior to the feeding trials and all of these butterflies displayed evidence of proboscis functionality. Butterflies with proboscides that did not reassemble also demonstrated fluid uptake capabilities, thus suggesting that wild butterflies might retain fluid uptake capabilities, even when the proboscis is partially injured.
Feeding Mechanisms of Adult Lepidoptera: Structure, Function, and Evolution of the Mouthparts
Annual Review of Entomology, 2010
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 foo...
Hydrophobic-hydrophilic dichotomy of the butterfly proboscis
Journal of The Royal Society Interface, 2013
Mouthparts of fluid-feeding insects have unique material properties with no human-engineered analogue: the feeding devices acquire sticky and viscous liquids while remaining clean. We discovered that the external surface of the butterfly proboscis has a sharp boundary separating a hydrophilic drinking region and a hydrophobic non-drinking region. The structural arrangement of the proboscis provides the basis for the wetting dichotomy. Theoretical and experimental analyses show that fluid uptake is associated with enlargement of hydrophilic cuticular structures, the legulae, which link the two halves of the proboscis together. We also show that an elliptical proboscis produces a higher external meniscus than does a cylindrical proboscis of the same circumference. Fluid uptake is additionally facilitated in sap-feeding butterflies that have a proboscis with enlarged chemosensory structures forming a brush near the tip. This structural modification of the proboscis enables sap feeders to exploit films of liquid more efficiently. Structural changes along the proboscis, including increased legular width and presence of a brush-like tip, occur in a wide range of species, suggesting that a wetting dichotomy is widespread in the Lepidoptera.
Journal of The Royal Society Interface, 2012
The ability of Lepidoptera, or butterflies and moths, to drink liquids from rotting fruit and wet soil, as well as nectar from floral tubes, raises the question of whether the conventional view of the proboscis as a drinking straw can account for the withdrawal of fluids from porous substrates or of films and droplets from floral tubes. We discovered that the proboscis promotes capillary pull of liquids from diverse sources owing to a hierarchical pore structure spanning nano-and microscales. X-ray phase-contrast imaging reveals that Plateau instability causes liquid bridges to form in the food canal, which are transported to the gut by the muscular sucking pump in the head. The dual functionality of the proboscis represents a key innovation for exploiting a vast range of nutritional sources. We suggest that future studies of the adaptive radiation of the Lepidoptera take into account the role played by the structural organization of the proboscis. A transformative two-step model of capillary intake and suctioning can be applied not only to butterflies and moths but also potentially to vast numbers of other insects such as bees and flies.
The hummingbird tongue is a fluid trap, not a capillary tube
Hummingbird tongues pick up a liquid, calorie-dense food that cannot be grasped, a physical challenge that has long inspired the study of nectar-transport mechanics. Existing biophysical models predict optimal hummingbird foraging on the basis of equations that assume that fluid rises through the tongue in the same way as through capillary tubes. We demonstrate that the hummingbird tongue does not function like a pair of tiny, static tubes drawing up floral nectar via capillary action. Instead, we show that the tongue tip is a dynamic liquid-trapping device that changes configuration and shape dramatically as it moves in and out of fluids. We also show that the tongue-fluid interactions are identical in both living and dead birds, demonstrating that this mechanism is a function of the tongue structure itself, and therefore highly efficient because no energy expenditure by the bird is required to drive the opening and closing of the trap. Our results rule out previous conclusions from capillarity-based models of nectar feeding and highlight the necessity of developing a new biophysical model for nectar intake in hummingbirds. Our findings have ramifications for the study of feeding mechanics in other nectarivorous birds, and for the understanding of the evolution of nectarivory in general. We propose a conceptual mechanical explanation for this unique fluid-trapping capacity, with far-reaching practical applications (e.g., biomimetics).
Nectar uptake in bats using a pumping-tongue mechanism
Many insects use nectar as their principal diet and have mouthparts specialized in nectarivory, whereas most nectar-feeding vertebrates are opportunistic users of floral resources and only a few species show distinct morphological specializations. Specialized nectar-feeding bats extract nectar from flowers using elongated tongues that correspond to two vastly different morphologies: Most species have tongues with hair-like papillae, whereas one group has almost hairless tongues that show distinct lateral grooves. Recent molecular data indicate a convergent evolution of groove- and hair-tongued bat clades into the nectar-feeding niche. Using high-speed video recordings on experimental feeders, we show distinctly divergent nectar-feeding behavior in clades. Grooved tongues are held in contact with nectar for the entire duration of visit as nectar is pumped into the mouths of hovering bats, whereas hairy tongues are used in conventional sinusoidal lapping movements. Bats with grooved tongues use a specific fluid uptake mechanism not known from any other mammal. Nectar rises in semiopen lateral grooves, probably driven by a combination of tongue deformation and capillary action. Extraction efficiency declined for both tongue types with a similar slope toward deeper nectar levels. Our results highlight a novel drinking mechanism in mammals and raise further questions on fluid mechanics and ecological niche partitioning.
Butterfly proboscis as a biomicrofluidic system
Bulletin of the American …, 2009
It looks amazing how butterflies and moths with their thin feeding trunk are being able to sip very thick liquids like nectar or animal extractions. Their sucking ability goes beyond that: one can observe butterflies and moths probing liquids from porous materials like fruit flesh or wet soils. This suggests that the suction pressure produced by these insects is sufficiently high. The estimates based on engineering hydraulic formulas show that the pressure can be greater than one atmosphere, i.e. it can be greater than that any vacuum pump could supply. In this experimental study, the principles of interfacial flows are used to carefully analyze the feeding mechanism of butterflies and moths. We document the feeding rates and proboscis behavior of Monarch butterflies (Danaus plexippus) in different situations: when butterfly feeds from droplets, from vials modeling floral cavities, and from porous materials modeling fruits, wet soils, or dung. Using high speed imaging and simple models, we propose a scenario of butterfly feeding which is based on capillary action. According to the proposed mechanism, the trunk of butterflies and moths works like a fountain pen where the air bubbles play a significant role in controlling fluid flow.