Ultrablack color in velvet ant cuticle

Abstract

We studied the ultrastructure of the ultrablack cuticle in Traumatomutilla bifurca, an enigmatic and visually striking species of velvet ants (Hymenoptera, Mutillidae). Using a combination of scanning electron microscopy (SEM), transmission electron microscopy (TEM), confocal laser scanning microscopy (CLSM), and optical spectroscopy, we conducted a comprehensive analysis of the cuticle to elucidate its unique optical properties. SEM imaging provided a detailed surface morphology, while TEM provided insights into the internal structure. CLSM showed that the cuticle exhibits no autofluorescence. Our findings reveal a highly specialized cuticle, characterized by microstructures that effectively minimize reflectance and enhance light absorption. Optical spectrometry confirmed the ultrablack nature of the cuticle, with the measured reflectance approaching minimal levels across a broad spectrum of wavelengths. Therefore, our study contributes to a deeper understanding of ultrablack biological materials and their potential applications in biomimetics.

Keywords: Hymenoptera; Mutillidae; animal coloration; biophotonics; insects; superblack; surface.

Figure 1

Examples of ultrablack colors in animals within their natural habitats. (A) Peacock spider (Maratus tasmanicus, Araneae: Salticidae) (© 2021 Henning Kallies), (B) bird-of-paradise (Lophorina niedda, Passeriformes: Paradisaeidae) (© 2022 Jes Lefcourt), (C) Gaboon viper (Bitis rhinoceros, Squamata: Viperidae) (By Justin Philbois), and (D) butterfly (Catonephele numilia, Lepidoptera: Papilionidae). Figures A and B were reproduced from https://www.inaturalist.org/observations/95228671 and https://www.inaturalist.org/observations/13984541, respectively, with permission from the respective authors. This content is not subject to CC BY 4.0. Figures C and D were reproduced from https://www.inaturalist.org/observations/131996241 and https://www.inaturalist.org/photos/17218853, respectively (published by iNaturalist, distributed under the terms of the Creative Commons CC0 1.0 Universal license).

Figure 2

Velvet ants (Traumatomutilla bifurca, Hymenoptera: Mutillidae) in their natural habitats. The images highlight the dark integument with contrasting patterns of black and white setae. The photos depicted in Figure 2 were adapted (cropped) from https://www.inaturalist.org/photos/62624578, https://www.inaturalist.org/photos/62624589, https://www.inaturalist.org/photos/62624582, and https://www.inaturalist.org/photos/62624568 (© 2020 shrike2, published by iNaturalist, distributed under the terms of the Creative Commons Attribution-Non Commercial 4.0 International License, https://creativecommons.org/licenses/by-nc/4.0/). This content is not subject to CC BY 4.0.

Figure 3

Reflectance spectra of ultrablack colors in the velvet ant Traumatomutilla bifurca (Hymenoptera: Mutillidae) (orange line) (original data), the butterfly Troides helena (Lepidoptera: Papilionidae) (purple line), the peacock spider Maratus karrie (Araneae: Salticidae) (green line), and the bird-of-paradise Drepanornis bruijnii (Passeriformes: Paradisaeidae) (blue line). The spectra of the spider and bird were obtained from [10] and that of the butterfly was obtained from [12]. The spectra of T. bifurca are derived from our study. The illustrations of velvet ant and bird-of-paradise were created using Adobe Photoshop. Butterfly image is from Insectpedia - stock.adobe.com. This content is not subject to CC BY 4.0. The image of the peacock spider was reproduced from https://www.inaturalist.org/observations/160699324 (© 2022 Donna Newton, published by iNaturalist, distributed under the terms of the Creative Commons Attribution-Non Commercial 4.0 International License, https://creativecommons.org/licenses/by-nc/4.0/). This content is not subject to CC BY 4.0.

Figure 4

Scanning electron microscopy (SEM) images of the cuticle surface of Traumatomutilla bifurca (Hymenoptera: Mutillidae). It exhibits a dense covering of spines and setae (A–F). The setae display an arrangement of slightly flattened filamentous structures (B, C, E, and F). The setae feature grooved nanostructure and are hollow (D), with no morphological distinction between white (B and C) and black (E and F) setae. Legend: St = setae; Rn = grooves on the bristles; i = hollow interior of the setae; Es = surface sculpturing; Ce = slightly flattened setae; Cf = spines. Scale bars: 1 mm in A, 400 µm in B, 200 µm in C, 4 µm in D, and 500 µm in E, 100 µm in F.

Figure 5

Scanning (A–D) and transmission (E and F) electron microscopy images of the cuticle structure of Traumatomutilla bifurca (Hymenoptera: Mutillidae). There is a complex structural arrangement of lamellar units (C and D), stacked on top of each other (E and F). There are also dark transverse bands that interconnect two consecutive longitudinal bands of the same lamellae (arrow), or of two separate lamellae (A and B). Legend: L = lamellae; P = pillars; R = rugosity of chitin fibers embedded in a protein matrix. Scale bars: 100 µm in A, 20 µm in B, 15 µm in C, 3 µm in D, 5 µm in E and 1 µm in F.

Figure 6

Scheme illustrating the functionality of the surface structure in Traumatomutilla bifurca (Hymenoptera: Mutillidae). Proposed mechanisms of structurally assisted absorption by surface sculpturing and setae, as light (yellow arrows) traverses through the dark pigmented cuticle and into the absorbing layer. Additionally, there is multiple scattering between protrusions and iterative absorption as light traverses through the cuticle at each lamella. Thus, the increased path length of light through lamellae may cause enhanced absorption.

Figure 7

Confocal laser scanning microscopy micrographs (maximum intensity projections) showing different types of autofluorescence exhibited by the cuticle. Blue regions contain resilin or some other proteins, while green, orange, and red structures represent different degrees of sclerotization. Black regions are presumably melanized. (A) The cuticle of the velvet ant Traumatomutilla bifurca shows no autofluorescence, while black setae show a very low signal (white arrows). (B) The autofluorescence in the white setae is whitish, which means that all of the wavelengths are present in the signal.

Figure 8

Thermal images of a female Traumatomutilla bifurca (Hymenoptera: Mutillidae). (A) Visible spectrum image, (B) thermal image of the animal before heating, (C) thermal image after 1 min of heating, and (D) thermal image after 2 min of heating.