Structural Origins of Coloration in the Spider Phoroncidia Rubroargentea
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Downloaded from http://rsif.royalsocietypublishing.org/ on September 18, 2018 Structural origins of coloration in the spider Phoroncidia rubroargentea rsif.royalsocietypublishing.org Berland, 1913 (Araneae: Theridiidae) from Madagascar Research Sarah Kariko1, Jaakko V. I. Timonen2,5, James C. Weaver3, Dvir Gur6, Carolyn Marks4, Leslie Leiserowitz7, Mathias Kolle8 and Ling Li9 Cite this article: Kariko S, Timonen JVI, Weaver JC, Gur D, Marks C, Leiserowitz L, Kolle 1Museum of Comparative Zoology, 2Harvard John A. Paulson School of Engineering and Applied Sciences, 3 4 M, Li L. 2018 Structural origins of coloration in Wyss Institute for Biologically Inspired Technology, and Center for Nano Sciences, Harvard University, Cambridge, MA 02138, USA the spider Phoroncidia rubroargentea 5Department of Applied Physics, Aalto University School of Science, Espoo 02150, Finland Berland, 1913 (Araneae: Theridiidae) 6Department of Physics of Complex Systems and Department of Molecular Cell Biology, and 7Department of from Madagascar. J. R. Soc. Interface 15: Materials and Interfaces, Weizmann Institute of Science, Rehovot 76100, Israel 8 20170930. Department of Mechanical Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA 9Department of Mechanical Engineering, Virginia Tech, Blacksburg, VA 24060, USA http://dx.doi.org/10.1098/rsif.2017.0930 LL, 0000-0002-6741-9741 This study investigates the structural basis for the red, silver and black Received: 11 December 2017 coloration of the theridiid spider, Phoroncidia rubroargentea (Berland, 1913) from Madagascar. Specimens of this species can retain their colour after sto- Accepted: 30 January 2018 rage in ethanol for decades, whereas most other brightly pigmented spider specimens fade under identical preservation conditions. Using correlative optical, structural and chemical analysis, we identify the colour-generating structural elements and characterize their optical properties. The prominent Subject Category: silvery appearance of the spider’s abdomen results from regularly arranged Life Sciences–Physics interface guanine microplatelets, similar to those found in other spiders and fish. The microplatelets are composed of a doublet structure twinned about the [021] axis, as suggested by electron diffraction. The red coloration originates from Subject Areas: chambered microspheres (approx. 1 mm in diameter), which contain struc- biomaterials, nanotechnology tured fluorescent material. Co-localization of the red microparticles on top of the reflective guanine microplatelets appears to enhance the red color- Keywords: ation. The spider’s thick cuticular layer, which encases its abdomen, varies spider, structural colour, guanine, Phoroncidia in its optical properties, being transparent in regions where only guanine reflectors are present, and tanned, exhibiting light absorption where the red microspheres are found. Moreover, colour degradation in some pre- served spider specimens that had suffered damage to the cuticular layer Authors for correspondence: suggests that this region of the exoskeleton may play an important role in Sarah Kariko the stabilization of the red coloration. e-mail: [email protected] Ling Li e-mail: [email protected] 1. Introduction Since Hooke and Newton in the seventeenth century, scientists have been inves- tigating the material structures and mechanisms creating the breathtaking spectrum of colours in Nature [1,2]. Typically, the focus has been on the colour- ful feathers of birds, including peacocks and birds-of-paradise [3,4], the iridescent elytra of beetles [5], and the brightly coloured wings of butterflies [6–8]. Recently, however, arachnids, especially spiders, have received increas- ing attention in terms of structural coloration [9–12]. Some spiders are Electronic supplementary material is available vividly coloured and patterned by utilizing a variety of coloration strategies and some species even display the capacity for dynamic colour change online at https://dx.doi.org/10.6084/m9. [13–18], providing intriguing models for investigating colour production in figshare.c.3999489. nature. Understanding the phenomena underlying structurally enhanced & 2018 The Author(s) Published by the Royal Society. All rights reserved. Downloaded from http://rsif.royalsocietypublishing.org/ on September 18, 2018 (a) (b) (d) 2 rsif.royalsocietypublishing.org (c) J. R. Soc. Interface (e) ( f ) 15 : 20170930 (g) PL PR AL AR 1 mm Figure 1. Information of distribution, habitat and overall appearance of P. rubroargentea (Berland, 1913). (a) Map of Madagascar. The white dot indicates the location of Ranomafana National Park. (b) Photo of the rainforest in Ranomafana National Park where P. rubroargentea have been found. (c) Photo of a live Phor- oncidia in the field (credit: Paul Bertner). (d) P. rubroargentea stored in ethanol for 40 years (14 600 days), which still retains the vibrant red colour (MCZ IZ 32022). Theridula emertoni (MCZ IZ 143122) (e) before and (f) after 220 days in 70% ethanol. (g) Multiple views of a P. rubroargentea examined in this study (CASENT 9057540): PL, posterior left; PR, posterior right; AL, anterior left; AR, anterior right. coloration in spiders can potentially provide new design cues originating from structures other than from guanine-based for the design of photonic devices [11,19] and offer insights reflectors are found in a few families, such as Theraphosidae into the biological function of such colours. (tarantulas) and Salticidae ( jumping spiders) [9,24]. Currently, it is known that spiders use multiple coloration In addition to structural coloration, spiders also use strategies (structural colour, pigmentation and fluorescence) pigments to create colours through the selective absorption for visual display, similar to those implemented by other of specific wavelengths of incident light. There are six animal groups. Structural colour is produced from the inter- common classes of biochromes (biological pigments) used action of light with nano- and microstructures, which results to produce colours in animals: melanins, carotenoids, ommo- in the spectrally selective reflection or scattering of light. One chromes, bilins, porphyrines and pterins [10,25]. Of these, of the most common optical displays in spiders that relies on ommochromes, melanins and bilins have been found in spi- this light interaction with nano/microscopic structures is ders [10,15,26–28], whereas the presence of porphryines, the silvery reflection or matt white appearance originated carotenoids and pterins in spiders has not yet been estab- from guanine crystals [12,20–22]. Similar to other groups lished [12,28]. Ommochromes are the primary biological (e.g. fishes, reptiles and other arthropods), spiders have pigment present in spiders and are responsible for the evolved a mechanism in which guanine is diverted from the yellows, reds, oranges, browns and blacks [15,29]. While mel- digestive tract and stored in specialized cells called guanocytes anin, which is responsible for many of the dark colours from under the cuticle of the abdomen, where they scatter and reflect reddish brown to black [30], was only recently detected in light [20–23]. A matte white appearance results from spiders by Hsiung et al. [31], further study is needed to prismatic-shaped guanine crystals, which can provide a understand how widely distributed this pigment is across canvas-like background for pigment-based colour [22]. By con- spider taxa [31]. Billins are a class of green pigments that trast, a silvery and specularly reflecting surface appearance have also been found in some spiders and are usually originates from microscopic platelet-shaped guanine crystals either concentrated in the exoskeleton or are present in the [12,20–22]. Spiders with a guanine-based silvery appearance haemolymph (blood) and visible through transparent cuticles are widespread across different families, ranging from tiny [26,32]. The carotenoid pigment class is usually associated dewdrop spiders in the genus Argyrodes (family: Theridiidae) with creating colours ranging from dark red to pale yellow, such as Argyrodes elevatus Taczanowski, 1873, to long jawed however these pigments are acquired through consuming spiders in the family Tetragnathidae, such as Tetragnatha mon- plants or herbivores, and among arachnids they have so far tana Simon, 1874 [21,22]. Spiders with structural colour only been found in some mites [12,33,34]. Downloaded from http://rsif.royalsocietypublishing.org/ on September 18, 2018 (a) 3 tanned black spines tanned rsif.royalsocietypublishing.org sclerites shimmery sclerites red region shimmery red region silver region J. R. Soc. Interface matte red region (b) 0.30 15 silver region (c) : 20170930 0.25 shimmery red region black region diffusive white standard 2 mm 0.20 0.15 reflection 0.10 0.05 0.5 mm 0 400 500 600 700 800 wavelength (nm) Figure 2. Optical properties of P. rubroargentea.(a) Dorsal (left) and posterior (right) view of a P. rubrargentea specimen with different regions of coloration indicated (CASENT 9057540). (b) Reflection spectra taken from three different regions: silver, shimmery red and black regions. The shaded areas represent the spread of original data (greater than 10 measurements for each type) and solid lines are the averaged data. The reflection strength of a diffuse white standard is shown for comparison (MCZ IZ 50966). (Inset) A top-viewed image of P. rubroargentea, where the circles indicate the regions of optical measurement (CASENT 9057540). (c) A high-magnification