Solar energy harvesting in the epicuticle of the oriental hornet (Vespa orientalis)
The Oriental hornet worker correlates its digging activity with solar insolation. Solar radiation passes through the epicuticle, which exhibits a grating-like structure, and continues to pass through layers of the exo-endocuticle until it is absorbed by the pigment melanin in the brown-colored cuticle or xanthopterin in the yellow-colored cuticle. The correlation between digging activity and the ability of the cuticle to absorb part of the solar radiation implies that the Oriental hornet may harvest parts of the solar radiation. In this study, we explore this intriguing possibility by analyzing the biophysical properties of the cuticle. We use rigorous coupled wave analysis simulations to show that the cuticle surfaces are structured to reduced reflectance and act as diffraction gratings to trap light and increase the amount absorbed in the cuticle. A dye-sensitized solar cell (DSSC) was constructed in order to show the ability of xanthopterin to serve as a light-harvesting molecule.
KeywordsOriental hornet Vespa orientalisCuticleDye-sensitized solar cellI–V measurementsAntireflectionLight trappingDiffraction grating
The pattern of activity of several species of wasps have been studied (Gaul 1952; Potter 1964; Edwards 1968; Iwata 1976), and they all have shown a similar mode of behavioral pattern. The greatest period of activity is in the early morning when the wasps leaving and entering the nest are nearly twice as active as for the remainder of the day. The latter period of time is characterized by a fairly constant activity with a sudden drop in the evening. The Oriental hornet, in contrast, shows a peak of activity in the middle of the day (Ishay et al. 1967). The number of Oriental hornet workers emerging from the nest entrance around noon is by two orders of magnitude greater than the number of those emerging in the morning or evening hours.
Materials and methods
Atomic force microscopy
The second dorsal gastral segment (brown) and the third dorsal gastral segment (yellow) were measured by atomic force microscopy (AFM, Molecular Imaging Pico Plus) with the use of PicoScan5 software. Scanning was performed in tapping mode in air, using NSC35/AIBS noncontact silicon probes purchased from MikroMasch. Results were analysed with the use of WsXM 5 software (Horcas et al. 2007).
Preparation of slices of exo-endocuticle for ESEM
Dorsal cuticular segments were immersed in liquid nitrogen then fractured to reveal their internal structure. The third dorsal gastral segment was from an Oriental hornet worker 3 days pre-eclosion and from a cuticle 3 days post-eclosion (to compare between morphological changes and reflectivity). The segments were fixed at 4°C in 3% (V/V) glutaraldehyde in phosphate buffered saline (PBS) overnight. After several washings in PBS, the tissue was postfixed in 1% OsO4 in PBS for 2 h. Dehydration was carried out in graded ethanol and embedding in glycid ether. Two micron sections were cut for observation. The cuticular sections were viewed via the Quanta 200 FEG environmental scanning electron microscope (ESEM). The samples were imaged with the secondary electron large-field detector [lateral force microscopy (LFM)] in low vacuum mode of 70 Pa as previously described (Plotkin et al. 2009a).
Reflectivity of cuticular stripes was measured on the double monochromator Lambda 900 UV/visible (VIS)/infrared (IR) spectrometer. The dual-channel scheme was used for conducting measurements: a front surface mirror with known reflectance was placed in a reference channel and samples were placed in a sample compartment. Measurements were conducted in a spectral range of 400–850 nm with a step of 1 nm. Measurement accuracy was about 1%.
The brown and yellow cuticle surfaces were modeled using rigorous coupled wave analysis (RCWA), implemented using a commercial software package (GD-Calc.; Nevière and Popov 2003; Johnson 2008). The surface structures of the two types of cuticle were recreated in GD-Calc using a staircase approximation, with 30 strata. The optical properties of the multilayer structure below the surface of the epicuticle are as yet unknown and so the full structure could not be modeled. We decided to concentrate on the effects that the top surface topography has on the incident light so in order to isolate these effects, a homogeneous substrate was used, rather than a multilayer. The refractive index of the epicuticle surface features and the homogeneous substrate was defined as 1.56 (i.e., of chitin). The medium above the epicuticle surface was defined with a refractive index of 1 (i.e., of air). GD-Calc was then used to calculate the diffraction efficiencies of each reflected order for transverse electric (TE or s) and transverse magnetic (TM or p) polarizations, for light incident normal to the surface, over a wavelength range from 400 to 850 nm, with an interval size of 5 nm. The maximum number of diffraction orders included in the calculations was 10, by which point convergence tests demonstrated that the solutions had converged. The diffraction efficiencies were summed to give a total reflectance for each wavelength, thus allowing the generation of reflectance versus wavelength plots and the antireflection (AR) properties of surface structure to be investigated.
To test the hypothesis that xanthopterin can act as an absorber material for solar radiation, a dye-sensitized solar cell (DSSC, O’Regan and Grätzel 1991) was constructed using the following method:
Mesoporous TiO2 films (12-μm-thick) were prepared by electrophoretic deposition (EPD; Grinis et al. 2008) of Degussa P25 particles with an average diameter of 25 nm onto fluorine-doped tin oxide (FTO) covered glass substrates (Pilkington TEC 15) with 15 Ω/square sheet resistances.
Films were deposited in four consecutive cycles of 60 s at a constant current density of 0.4 mA/cm2 (which corresponded to 70 V at an electrode distance of 50 mm), and dried at 120°C for 5 min in between cycles. Following the EPD process, all the electrodes were dried in air at 150°C for 30 min, pressed under 800 kg/cm2 using a hydraulic press, and sintered at 550°C for 1 h. The thickness of the mesoporous electrodes was measured with a profilometer (Surftest SV 500, Mitutoye). The electrodes were subsequently immersed in 1 mM of xanthopterin in ethanol for 24 h and then rinsed with ethanol. An I-/I3-redox electrolyte was used in the xanthopterin-sensitized solar cell, consisting of 0.1 M lithium iodide, 0.05 M iodine, 0.6 M 1-propyl-2,3 dimethylimidazolium iodide, and 0.5 M 4-tertbutylpyridine dissolved in a solution of acetonitrile and 3-methoxypropionitrile at a ratio of 1:1. A Pt-coated FTO glass was used as a counterelectrode. Photocurrent–voltage characteristics were performed with an Eco-Chemie Potentiostat using a scan rate of 10 mV/s. A 250 W xenon arc lamp (Oriel) calibrated to 100 mW/cm2 (AM 1.5 spectrum) served as a light source. The illuminated area of the cell was 0.64 cm2.
DSSCs provide a technically and economically credible alternative concept to crystalline silicon-based p–n junction photovoltaic devices. In contrast to conventional systems, where light absorption and charge carrier transport takes place in the semiconductor, these two processes are separated in DSSCs. Light is absorbed by a sensitizer which is anchored to the surface of a mesoporous wide band gap semiconductor film (usually TiO2). Charge separation takes place at the dye/semiconductor interface via a two-step photo-induced process. First, an electron is excited from the HOMO to the LUMO level of the dye, followed by injection into the conduction band of the semiconductor. After charge separation, electrons diffuse through the mesoporous semiconductor toward a conducting transparent front electrode, while positive charges are transported by the electrolytes’ redox species to a Pt back electrode.
We have shown through RCWA simulations that the epicuticle acts as an antireflective layer. As a comparison, nipple arrays, such as those found on the eyes and wings of some species of moth, confer also an antireflective effect (Bernhard 1967; Parker 2000; Vukusic and Sambles 2003). With periods of ~200 nm, the moth-eye structures are on a scale below the wavelength range of solar radiation, which means they act as an effective medium, with an effective refractive index that changes gradually across the interface. With periods of ~500 nm, the structures on the brown and yellow epicuticles are not subwavelength across the solar spectrum and so do not act as a true effective medium in the same way as the moth-eye structures. Therefore, although conferring some antireflective effect, the surface structures observed on the Oriental hornet cuticles are far from optimized for this purpose. However, unlike the moth-eye arrays, which are too small to diffract light, the brown cuticle structure also acts as a diffraction grating, enhancing light trapping and so absorption within the cuticle. The 5.1% increase in absorption calculated for the brown epicuticle structure compared to a flat surface is likely to be an underestimate because it only accounts for one pass through the cuticle; the 1 and −1 orders are travelling at higher angles and so more of the light will undergo internal reflection at the back surface and pass through the cuticle a second time, resulting in even more absorption compared to a flat surface. These findings suggest the possibility that the surface structure has evolved to confer both AR and light-trapping properties to the epicuticle, enhancing the absorption of light within the cuticle of the hornet, resulting in more efficient collection of solar energy. Results of the optical modeling do not match the measured reflectance because they do not take into account the underlying layered structure; instead, it is assumed that the surface structure is formed in a semi-infinite chitin substrate. The Oriental hornet exo-endocuticle comprises a series of thin sheet-like structures, stacked on top of each other, with decreasing thickness from top to bottom (Fig. 3a). In every layer, there is circular rod-like structure composed of chitin chains packed together (Fig. 3b, arrows). The rods of chitin are embedded in a protein matrix (Giraud-Guille and Bouligand 1986; Fig. 3b, M). The large differences between the measured (Fig. 4) and simulated (Fig. 5) reflectance results demonstrate that this underlying layered structure contributes to the overall reflectance properties of the epicuticle. The effective refractive index of the chitin rods and the protein matrix combined in each layer of the Oriental hornet cuticle is still unknown. The orientation of the rods in each layer and the impact of this orientation on the refractive index in each layer are still unclear, those questions will be elucidated in future studies. It is possible that the underlying layered structure introduces a gradual change in effective refractive index by varying the proportion of chitin and protein in each layer. Such an approach has been used by solar cell designers who have formed layers of nanorods, whereby the refractive index is controlled by changing the portion of air in each layer or by altering the angle of deposition of the nanorods (Chhajed et al. 2008; Kuo et al. 2008). Additionally, the Oriental hornet oval body structure means that the solar angle of incidence changes along its body, which may impact on the amount of light reflected. This problem could have been solved by the hornet by utilizing what may be an omnidirectional antireflective structure. Light passing through the yellow stripes is absorbed by xanthopterin, which serves as a light-harvesting molecule. The xanthopterin resides in tightly packed yellow pigment granules, which may serve to increase the effective surface area available for light absorption. Pterins are found in high concentrations in pierid butterflies (Wijnen et al. 2007). Pterins are housed in similar granular formation (beads) which allow absorption in the UV wavelengths while allowing an increase in the reflectance of higher wavelengths (Stavenga et al. 2004). The ability of xanthopterin to serve as a visible light absorber in a photo electrochemical solar cell is clearly evident from the I–V characteristics of the xanthopterin-sensitized solar cell. Previous studies have shown diffusion potential across the cuticle, with the inside negative with respect to the outside. Digby (1965) has suggested that electrons move through the semiconductive cuticular layer. This process creates calcium carbonate that precipitates in the cuticle. In conclusion, we have presented evidence supporting the hypothesis that the Oriental hornet has evolved a cuticle design to harvest solar energy. RCWA simulations show that the surface structures confer AR and light-trapping properties, enhancing absorption by approximately 5% compared to a flat surface. The xanthopterin pigment found within the cuticle has been proven to be a suitable absorber of light for the harvesting of solar energy by a demonstration of its use in an organic solar cell, with a conversion efficiency of 0.335%. Future work will focus in investigating the complex layered structure observed in the cuticle cross-sections, and its possible role in solar energy harvesting.
The authors would like to thank the Bio-AFM Laboratory Manager, Dr. Artium Khatchatouriants, from the Center for Nanoscience and Nanotechnology at Tel Aviv University for his help and advice. We would like to thank Dr. Vered Holdengreber from the Electron Microscopy Unit, IDRFU Life Sciences at Tel-Aviv University for her help in the preparation of the cuticular slices of the exo-endocutile for ESEM analysis. This work was performed in partial fulfillment of the requirements for a PhD degree of Marian Plotkin.
Conflicts of interest