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. 2019 Dec 24;9(1):19731.
doi: 10.1038/s41598-019-56203-6.

An Augmented Wood-Penetrating Structure: Cicada Ovipositors Enhanced With Metals and Other Inorganic Elements

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Free PMC article

An Augmented Wood-Penetrating Structure: Cicada Ovipositors Enhanced With Metals and Other Inorganic Elements

Matthew S Lehnert et al. Sci Rep. .
Free PMC article

Abstract

Few insect species are as popular as periodical cicadas (Magicicada spp.). Despite representing an enormous biomass and numbers that exceed 370/m2 during mass emergences, the extended time period of the underground nymphal stages (up to 17 years) complicates investigations of their life history traits and ecology. Upon emergence, female cicadas mate and then use their ovipositors to cut through wood to lay their eggs. Given the ability to penetrate into wood, we hypothesized that the ovipositor cuticle is augmented with inorganic elements, which could increase hardness and reduce ovipositor fracturing. We used scanning electron microscopy and energy dispersive x-ray spectroscopy to evaluate the material properties of ovipositors of four cicada species, including three species of periodical cicadas. We found 14 inorganic elements of the cuticle, of which P, Ca, Si, Mg, Na, Fe, Zn, Mn, Cl, K, and S show the highest concentrations (%wt) near the apex of the ovipositor, where other structural modifications for penetrating wood are present. To the best of our knowledge, this is the first report of metal deposits in the cuticle of true bugs (Hemiptera, >80,000 described species).

Conflict of interest statement

The authors declare no competing interests.

Figures

Figure 1
Figure 1
Morphology of cicada ovipositors and the rasping regions. (ad) are illustrations of cicada ovipositors and their corresponding rasping regions are shown as SEM images on the right side. (a,b) show the ventral side and dorsal side of the ovipositor of N. linnei and (c,d) show the ventral and dorsal side of M. cassinii, respectively. All studied ovipositors consist of medial gonapophyses IX (GIX) and lateral gonapophyses VIII (GVIII). The GVIII covers the lateral sides of the GIX and wraps around the ventral side, covering the entire GIX except at the distal end. The ventral side of the GVIII has lobes (Lo) near the distal tip, which represents where the eggs exit the ovipositor. The medial region of a GIX has ridges (Ri) that interlock with ridges from the other GIX. All studied ovipositors have a rasping region with teeth (singular = tooth, To). The ovipositors were illustrated by Brooke Pandrea.
Figure 2
Figure 2
SEM images of the teeth of cicada ovipositors. (a,b) show the dorsal side of the rasping region of the ovipositor of M. septendecula and N. linnei, respectively. A tooth (To) consists of two structurally-defined regions, a smooth (Sm) distal part and a rough (Ro) proximal region. The dorsum of the rasping teeth of N. linnei (b) have a knob-like protrusion (Pr). Ventral images of ovipositors of M. septendecim (c) and N. linnei (d) show that the teeth are bump-like laterally and have campaniform sensilla (Se), which were observed in all studied species.
Figure 3
Figure 3
Ovipositor structures associated with the sliding mechanism. (a,b) show that the gonapophyses IX (GIX) have grooves (Gr) that fit onto the gonapophyses VIII (GVIII), allowing the GVIII to make anti-parallel movements along the GIX. The GVIII are capable of sliding distally, past the GIX (c), or sliding proximally, exposing the distal part of the GIX (d). The GIX have ridges (Ri) that are tooth-like in the distal regions (e) and more plate-like in proximal regions (f), which likely stabilize the GIX while the GVIII are performing anti-parallel movements to penetrate wood for subsequent oviposition.
Figure 4
Figure 4
Plot of EDS values averaged across species for the elements K (a), S (b), Cl (c), and Mn (d) on the dorsal surface of the ovipositor. Bars (X¯ + SE) are plotted in their approximate proximal to distal sampling location along the ovipositor (x-axis). Sampling points 9 and 10 are proximal, sampling points 7 and 8 are mid-ovipositor, and sampling points 1–6 are distal (see Fig. 2 for sampling locations). The EDS values for each species were averaged together per location and tested for significant differences among proximal to distal location groupings at the α = 0.05 level (significant differences are represented by lowercase letters). Mn was not detected in M. septendecula on the dorsal surface; therefore, that bar is not shown in graph D nor was Mn included in the tests for significant differences. Note that the y-axis has a different scale for each element.

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