Penetration mechanics of a beetle intromittent organ with bending stiffness gradient and a soft tip

Matsumura, Yuichi; Kovalev, Alexander; Gorb, Stanislav N.

doi:10.1126/sciadv.aao5469

Cited by 28 publications

(44 citation statements)

References 58 publications

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“…The model was used to test whether the obtained Young's moduli could be used to reproduce the behaviour of the flagellum under loading. We simulated the three-point bending tests conducted by Matsumura et al [31] (figure 3c). Figure 3d presents the displacement of our model and that of the biological flagellum under the same loading condition.…”

Section: Resultsmentioning

confidence: 99%

“…In order to measure the stiffness of the male flagellum of the beetle Cassida rubiginosa, Matsumura et al [31] conducted threepoint bending tests (figure 3c). In their experiments, the proximal part of the flagellum with a length of 300 -340 mm was placed between two insect pins.…”

Section: Bending Of the Flagellummentioning

confidence: 99%

“…We test the validity of the obtained moduli for two other insect cuticles having completely different geometries and material gradients: the male flagellum of the beetle Cassida rubiginosa and the hindleg tibia of the stick insect Carausius morosus. These examples were selected because experimental data on their mechanical behaviour under loading are available in the literature [30,31].…”

Section: Introductionmentioning

confidence: 99%

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A simple, high-resolution, non-destructive method for determining the spatial gradient of the elastic modulus of insect cuticle

Eshghi¹,

Jafarpour

Darvizeh

et al. 2018

J. R. Soc. Interface.

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Nature has evolved structures with high load-carrying capacity and long-term durability. The principles underlying the functionality of such structures, if studied systematically, can inspire the design of more efficient engineering systems. An important step in this process is to characterize the material properties of the structure under investigation. However, direct mechanical measurements on small complex-shaped biological samples involve numerous technical challenges. To overcome these challenges, we developed a method for estimation of the elastic modulus of insect cuticle, the second most abundant biological composite in nature, through simple light microscopy. In brief, we established a quantitative link between the autofluorescence of different constituent materials of insect cuticle, and the resulting mechanical properties. This approach was verified using data on cuticular structures of three different insect species. The method presented in this study allows three-dimensional visualisation of the elastic modulus, which is impossible with any other available technique. This is especially important for precise finite-element modelling of cuticle, which is known to have spatially graded properties. Considering the simplicity, ease of implementation and high-resolution of the results, our method is a crucial step towards a better understanding of material-function relationships in insect cuticle, and can potentially be adapted for other graded biological materials.

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Section: Resultsmentioning

confidence: 99%

Section: Bending Of the Flagellummentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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A simple, high-resolution, non-destructive method for determining the spatial gradient of the elastic modulus of insect cuticle

Eshghi¹,

Jafarpour

Darvizeh

et al. 2018

J. R. Soc. Interface.

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show abstract

“…Similarly, few studies focus on the structural and material properties of the probe. These can be obtained with high-resolution CT imaging or sequential transmission electron microscopy (TEM), using X-ray diffraction (Blackwell & Weih, 1980), small-scale three-point bending (Matsumura, Kovalev & Gorb, 2017), or nano-indentation experiments (Politi et al, 2012). Due to the extremely small size of the probes, all these methods are either very expensive, difficult to execute, or both.…”

Section: Discussionmentioning

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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“…To our knowledge, this the first time that a modified composite profile has been reported as a means of enhancing structural elasticity in the insect exoskeleton (though see ref. ). The degree to which changes in laminate organization can alter the behavior of the cuticle also has dramatic implications for finite element modeling of insect exoskeletons, which often rely upon assumed isotropy and homogeneous composition of the cuticle.…”

mentioning

confidence: 97%

Avoidance of Catastrophic Structural Failure as an Evolutionary Constraint: Biomechanics of the Acorn Weevil Rostrum

et al. 2019

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The acorn weevil (Curculio Linnaeus, 1758) rostrum (snout) exhibits remarkable flexibility and toughness derived from the microarchitecture of its exoskeleton. Modifications to the composite profile of the rostral cuticle that simultaneously enhance the flexibility and toughness of the distal portion of the snout are characterized. Using classical laminate plate theory, the effect of these modifications on the elastic behavior of the exoskeleton is estimated. It is shown that the tensile behavior of the rostrum across six Curculio species with high morphological variation correlates with changes in the relative layer thicknesses and orientation angles of layers in the exoskeleton. Accordingly, increased endocuticle thickness is strongly correlated with increased tensile strength. Rostrum stiffness is shown to be inversely correlated with work of fracture; thus allowing a highly curved rostrum to completely straighten without structural damage. Finally, exocuticle rich invaginations of the occipital sutures are identified both as a likely site of crack initiation in tensile failure and as a source of morphological constraint on the evolution of the rostrum in Curculio weevils. It is concluded that avoidance of catastrophic structural failure, as initiated in these sutures under tension, is the driving selective pressure in the evolution of the female Curculio rostrum.

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Penetration mechanics of a beetle intromittent organ with bending stiffness gradient and a soft tip

Abstract: An apical region of a hyper-long penis in a beetle has flexibility gradient aiding in penetration of a coiled female duct.

Cited by 28 publications

References 58 publications

A simple, high-resolution, non-destructive method for determining the spatial gradient of the elastic modulus of insect cuticle

A simple, high-resolution, non-destructive method for determining the spatial gradient of the elastic modulus of insect cuticle

Functional principles of steerable multi‐element probes in insects

Avoidance of Catastrophic Structural Failure as an Evolutionary Constraint: Biomechanics of the Acorn Weevil Rostrum

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