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. 2019 May 31;16(154):20190049.
doi: 10.1098/rsif.2019.0049.

Material Stiffness Variation in Mosquito Antennae

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Free PMC article

Material Stiffness Variation in Mosquito Antennae

B D Saltin et al. J R Soc Interface. .
Free PMC article

Abstract

The antennae of mosquitoes are model systems for acoustic sensation, in that they obey general principles for sound detection, using both active feedback mechanisms and passive structural adaptations. However, the biomechanical aspect of the antennal structure is much less understood than the mechano-electrical transduction. Using confocal laser scanning microscopy, we measured the fluorescent properties of the antennae of two species of mosquito- Toxorhynchites brevipalpis and Anopheles arabiensis-and, noting that fluorescence is correlated with material stiffness, we found that the structure of the antenna is not a simple beam of homogeneous material, but is in fact a rather more complex structure with spatially distributed discrete changes in material properties. These present as bands or rings of different material in each subunit of the antenna, which repeat along its length. While these structures may simply be required for structural robustness of the antennae, we found that in FEM simulation, these banded structures can strongly affect the resonant frequencies of cantilever-beam systems, and therefore taken together our results suggest that modulating the material properties along the length of the antenna could constitute an additional mechanism for resonant tuning in these species.

Keywords: Anopheles; Toxorhynchites; antennal hearing; confocal laser scanning microscopy; finite-element modelling; mating behaviour.

Conflict of interest statement

We have no competing interests.

Figures

Figure 1.
Figure 1.
Schematic of antenna morphology. (a) Head of T. brevipalpis. (b) Cross section of the pedicel scale bar 0.1 mm. (c) Schematic of the inside of the pedicel (b,c) from Yack [15], simplified and modified. Image abbreviations: bp, basal plate; fb, fibrillae; fl, flagellum; pd, pedicel; pdw, pedicel wall; pr, prongs; s, scape.
Figure 2.
Figure 2.
Three-dimensional representation of our antenna model. This figure correlates modelling terminology with morphological terms. The antenna comprises 13 segments with 12 joints. In a model for T. brevipalpis, the antennal structure is a sequence of relatively hard long elements, interspersed with a series of three small elements of one soft material sandwiched between two hard small elements (figure 3a,b). In contrast in Anopheles, the antennal structure is a sequence of soft elements, separated by thin discs of hard material (figures 3c,d and 4). Points used for simulations in figure 6 are shown in red. To simulate an impinging sound field, a load was applied perpendicular to the beam axis in the +X direction on elements 2–13. Image abbreviations, with morphological terms in brackets if applicable: ‘bd’ basal disc (approximating the pedicellar articulation); fl, beam (flagellum); j, three small elements (joint); sg, long element (segment).
Figure 3.
Figure 3.
CLSM-based maximum intensity projections of the male antennae of T. brevipalpis (a,b) and An. arabiensis (c,d). Higher resolution images available in the electronic supplementary material. (a) Antenna, with increased brightness, showing the 12 more-or-less regular subunits and a varying 13th one. Inset: Zoomed image of bands of a different individual. (b,c) Comparison image of (b) T. brevipalpis. (2nd segment) and (c) An. arabiensis (4th to 8th segment), with increased brightness. The antenna of T. brevipalpis is larger and thicker. It is made up of relatively stiff cuticle with small, relatively flexible (blue) and hard (red/orange) rings, while An. arabiensis antenna is made up of relatively soft (light blue) cuticle interspaced with hard rings. In both species, the area where the fibrillae emerge is hard (orange). In (a,b) (T. brevipalpis), the image shows two red-orange discs sandwiching a blue disc at the base of the segments (white arrow). (d) Overview of An. arabiensis with increased brightness. The overall anatomy is dominated by relatively soft and flexible areas, interspaced with comparatively hard bands where fibrillae insert. Image abbreviations: fb, fibrillae; fl, flagellum; j, joint; pd, pedicel (grey arrowhead in (d)); rs, ring structure; sg, segment.
Figure 4.
Figure 4.
Maximum intensity projection of An. arabiensis, with increased brightness, showing detail of two flagellomeres and the insertion position of fibrillae. Males of this species can erect the fibrillae depending on diurnal cycle and activity, due to the presumably soft, sac-like structure that is outlined by the granulae (gr) below the hard ring structure (rs). The combination of these two structures can potentially provide the mechanical basis to inflate by hydraulic pressure and erect the fibrillae. Fibrillae sockets on the ring structure (white arrowheads) are where the fibrillae insert. Image abbreviations: fb, fibrillae; fl, flagellum; gr, granulae; j, joint; pd, pedicel; rs, ring structure; sg, segment. *Deep-blue fluorescent small band, **yellow-orange fluorescent band.
Figure 5.
Figure 5.
CLSM images of a T. brevipalpis male that shows a maximum intensity projection of an opened pedicel. This attachment is comparatively hard (red arrowhead) and the prongs run over a ridge (white arrowhead), which appears as hard as the prongs themselves. Image abbreviations: pdw, pedicel outer wall; pr, prongs; rg, ridge (white arrowhead).
Figure 6.
Figure 6.
Simulation results. For a modelled beam, (a) shows the change of frequency response over four orders of magnitude of base stiffness, and (b) shows the effect of adding hard or soft elements to a uniform beam with base stiffness of 10 kPa as in figure 2. Overlaid are dashed curves indicating simulations where both hard and soft elements are added—in this case 10× harder elements in combination with 10×, 100× and 1000× softer elements—colour-coded as for soft elements. (c) Comparison of a Toxorhynchites-type model with either uniform stiffness, or hard and/or soft elements added. Only the addition of soft elements appreciably affects the frequency response. Note that the resonance is consistent with wingbeat frequencies in this species. (d) Comparison of the Anopheles-type model with either uniform stiffness or the addition of hard elements. Hard elements increase the resonant frequency.

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