Comparative Material and Mechanical Properties among Cicada Mouthparts: Cuticle Enhanced with Inorganic Elements Facilitates Piercing through Woody Stems for Feeding

Abstract

Adult cicadas pierce woody stems with their mouthparts to feed on xylem, suggesting the presence of cuticular adaptations that could increase hardness and elastic modulus. We tested the following hypotheses: (a) the mouthpart cuticle includes inorganic elements, which augment the mechanical properties; (b) these elements are abundant in specific mouthpart structures and regions responsible for piercing wood; (c) there are correlations among elements, which could provide insights into patterns of element colocalization. We used scanning electron microscopy (SEM) and energy dispersive X-ray spectroscopy (EDS) to investigate mouthpart morphology and quantify the elemental composition of the cuticle among four cicada species, including periodical cicadas (Magicicada sp.). Nanoindentation was used to quantify hardness and elastic modulus of the mandibles. We found 12 inorganic elements, including colocalized manganese and zinc in the distal regions of the mandible, the structure most responsible for piercing through wood; nanoindentation determined that these regions were also significantly harder and had higher elastic modulus than other regions. Manganese and zinc abundance relates to increased hardness and stiffness as in the cuticle of other invertebrates; however, this is one of the first reports of cuticular metals among insects with piercing-sucking mouthparts (>100,000 described species). The present investigation provides insight into the feeding mechanism of cicadas, an important but understudied component of their life traits.

Diverse material properties and morphology of moth proboscises relates to the feeding habits of some macromoth and other lepidopteran lineages

“…The material properties of insect structures play an important role in their functionality [18,21,59]. Elasticity of the insect cuticle, for example, is often associated with the presence or absence of resilin [22,50,60].…”

“…Insect mouthparts provide compelling examples of structure and function relationships and support important components of natural selection, including convergent evolution [4,5] and coevolution [1,6,7]. Studies of insect mouthparts have become more interdisciplinary, often involving fields that span morphology [8][9][10], biomechanics [11][12][13], developmental biology [14,15], material sciences [16][17][18] and chemistry [19][20][21]. Although mouthparts have been studied from an array of insect lineages, the lepidopteran proboscis has notably experienced an increase in study abundance [22], likely due to their large biodiversity, important role as pollinators, and interesting feeding mechanism that is capable of transporting nanolitres of liquids from wetted surfaces to the gut [23].…”

Mandible elemental composition and mechanical properties from distinct castes of the leafcutter ant Atta laevigata (Attini; Formicidae)

“…Even though the insect cuticle lacks a higher content of minerals, transition metals (Cu, Fe, Mn, Zn), with colocalized halogens (Cl) and alkaline earth metals (Ca, Mg) were additionally found to be abundant in structures prone to structural failure or wear, such as mouthparts [ 23 , 28 , 29 , 31 – 34 , 41 , 48 , 49 , 61 , 76 – 83 ]. Cu, Fe, Mn and/or Zn ions probably serve as cross-links [ 41 , 61 , 80 , 84 – 87 ], whereas Ca and Mg could be present in crystalline form [ 34 , 43 – 45 ].…”

Mechanical and elemental characterization of ant mandibles: consequences for bite mechanics

“…A higher degree of cuticular H and E along the mandible masticatory margin is commonly observed in ants (Brito et al 2017;Schofield et al 2002;2021), although only a few species were measured so far, mainly leaf-cutter ants. Such higher levels of material properties along the masticatory margin usually follow the concentration of transition metals like Zn (Schofield et al 2021), which tend to concentrate along the cutting edge or other cutting and piercing tools of arthropods (Polidori et al 2020;Schofield et al 2021;Krings & Gorb 2023;Reiter et al 2023;Krings & Gorb 2023). In leaf cutter ants, the mandible cutting edge is usually stiffer and harder (Schofield et al 2002;2021), which could be a mechanism to deal with the abrasion associated with the behavior of cutting leaves, as well as to improve the selfsharpening mechanism of such a structure (Martínez et al 2020).…”

“…Transition and alkaline earth metals in the cuticle are observed in several arthropod lineages, especially on appendages associated with biting or puncture, like spider fangs (Politi et al 2021;Schofield et al 2021), scorpion claws, pedipalps, and chelicerae (Schofield et al 2003;Schofield et al 2021), mandibles of termites (Cribb et al 2007), cicadas (Reiter et al 2023), ant lions (Krings & Gorb 2023), and ants (Schofield et al 2002;2021;Polidori et al 2020). Along with these cross-links, it is known that ant species can incorporate minerals into their cuticle , similar to the cuticles of crustaceans.…”