Color production mechanisms in spiders.
CONTENTS 1. Introduction 165 2. Absorption 166 2.1. Melanins 166 2.2. Carotenoids 166 2.3. Ommochromes 167 2.4. Bilins 168 2.5. Pterins 168 3. Scattering 168 3.1. Guanine crystals 169 3.2. Disordered structures 170 3.3. Amorphous spongy structures (photonic glasses) 170 3.4. Multilayer structures 171 3.5. Photonic crystals 171 3.6. Diffraction gratings 172 4. Emission 172 5. Color by interaction of multiple mechanisms 173 5.1. Pigmentary--structural color interaction 173 5.1.1. Color mixing 173 5.1.2. Light absorbing backgrounds 173 5.1.3. Light reflecting backgrounds 174 5.2. Interactions between structural elements across different spatial scales 174 5.3. The interaction between order and randomness 175 6. Conclusions 176
Although the majority of spiders are relatively dull and drab in coloration, many are vividly colored. These colors serve important functions for spiders, ranging from prey attraction, camouflage, aposematism, and thermoregulation, to species recognition and courtship display. Hence, color is obviously interesting to researchers studying spider behavior, ecology, and evolution (for reviews regarding these topics, see Oxford & Gillespie 1998 and Nentwig 2013, as the scope of our review article is focused mainly on color production mechanisms). Recent studies provide substantial insight into the proximate mechanisms of how spiders produce these colors. Therefore, it is timely to examine color production mechanisms in spiders in a more systematic way, to synthesize the available literature regarding color mechanisms and to pave the way for future advances in the field.
Color perception in animals arises through an interaction between light and neural processing. Here, we focus on the first part of that interaction and define color as the physical composition of light that reaches the receivers, which can be measured using a spectrophotometer. A color is therefore produced by light-matter interactions, either by removing a portion of the ambient spectral composition through pigment absorption (i.e., pigmentary color), by scattering only specific wavelengths of ambient light back to the receiver through structures with sub-micrometer size features (i.e., structural color), or by a combination of the two. Finally, color can also be produced by actively emitting light through the process of fluorescence or bioluminescence. In this review, we emphasize spider structural colors because pigmentary colors have been summarized many times in the literature (Oxford & Gillespie 1998; Foelix 2011) so that we only discuss recent advances in spider pigmentary color. We still know very little about spider fluorescence and thus will not address it in detail. No example of bioluminescence in spiders has been found so far.
We first summarize the current understanding of how colors are produced in spiders. Second, we propose candidate spider species for further investigation based on knowledge of color production mechanism from other organisms. Finally, we discuss how colors in spiders differ from those in other organisms. We hope that this review will guide future research on both proximate and ultimate mechanisms of color production.
Pigments absorb specific wavelengths of light when the energy of photons at these wavelengths equals the energy required to transfer electrons from a lower energy level to a higher energy level in the pigments' molecular orbitals (Zollinger 2003). This electron transition usually happens between the highest occupied molecular orbital (HOMO) and the lowest unoccupied molecular orbital (LUMO), and the energy required is mostly determined by the chemical structure of the pigment. Consequently, different pigments absorb various portions of the spectrum, producing diverse colors based on their individual chemical structures. The color produced by a pigment is non-iridescent, meaning that its hue does not change with viewing or illumination direction. Pigments are probably the most common color production mechanism in nature, and likely also the best studied. However, our knowledge of spider pigments is still limited relative to other organisms. Here, we discuss some of the more widespread classes of pigments in animals, such as melanins, carotenoids, and ommochromes. For other more lineage-specific, and minor classes of pigments, we only include the pigments that have already been identified in spiders (e.g., bilin), and the pigments speculated to be present in spiders (e.g., pterin).
2.1 Melanins.--Melanins have many important biological functions, and may serve non-coloration functions like photoprotection (Brenner & Hearing 2008), microbial resistance (Krams et al. 2016), and mechano-enhancement of cuticle sclerotization in insects (Riley 1997). Although melanin is widely spread across all living organisms, it has only recently been found in spiders (Hsiung et al. 2015a).
Based on the chemical structures of melanin, it can be divided into black-producing eumelanin (Fig. 1A), and dark reddish-brown-producing pheomelanin. Hsiung (2015a) detected eumelanin signature signals in all spiders that they surveyed (fourteen species across six families) using Raman spectroscopy. Raman spectroscopy may also distinguish eumelanin from pheomelanin (GalvEin et al. 2013). However, pheomelanin Raman signals may be inconspicuous in raw spectra, and require post-acquisition processing, such as baseline correction, to be detected. In a previous genomic study, twelve out of nineteen genes associated with melanin synthesis in Drosophila melanogaster were not found in spiders (Croucher et al. 2013), suggesting that spiders may use different enzymes or substrates to synthesize eumelanin. A recent study also suggested that insects utilize enzymes and substrates different from that of mammals to synthesize both eu- and pheo-melanin (Barek et al. 2017). Whether pheomelanin is present in spiders or not remains to be determined.
Melanosomes are organelles that produce and contain melanin, and they often organize in ways that produce vibrant structural colors. Melanosomes were recently found in spiders (Hsiung et al. 2017a). Thus far, this is the only known example of melanosomes in invertebrates. Melanosomes occur in a randomly packed formation in the hypodermis of the Australian peacock spiders (Maratus spp., Salticidae), and may function to absorb scattered light and thereby increase structural color saturation (Kinoshita et al. 2002). However, birds organize melanosomes in nanostructures to produce brilliant structural colors, and whether spiders also use melanosomes to control the hue of color signals remains to be seen.
Many species of wolf spiders in the genus Schizocosa have melanin-based black ornamental tufts of bristles (Hsiung et al. 2015a) on the tibia of their forelegs, and use them in the visual displays during the courtship rituals (Hebets & Uetz 2000; Vaccaro et al. 2010). Could melanin act as honest signals in spiders, as suggested in some birds (Jawor & Breitwisch 2003; D'Alba et al. 2014)? Experiments should be devised to test these functional hypotheses in the spider groups with competent vision in the future.
2.2 Carotenoids.--Carotenoids produce a series of colors ranging from light yellows and oranges to dark reds. Most animals cannot synthesize carotenoids de novo, and must acquire carotenoids via diet (Fox 1976). Therefore, colors produced by carotenoids are often hypothesized to be honest signals for health and/or foraging ability (Lintig et al. 2005). Although carotenoids are well characterized across animals (Goodwin 1984, 1986), they were only recently identified in spiders (Hsiung et al. 2017a). We found that all carotenoids identified so far in spiders produce yellow coloration (Fig. 1B). One possible explanation is that spiders lack the enzymes that convert yellow dietary carotenoids to orange/red ketocarotenoids. Animals that produce orange/red carotenoid colors either evolved these carotenoid conversion enzymes independently, as in crustaceans, insects, fishes (Goodwin 1984, 1986), turtles and birds (Twyman et al. 2016); or acquired the genes necessary to produce carotenoids de novo through horizontal gene transfer from fungi, such as in mites (Grbic et al. 2011). While most studies have assumed that enzymes responsible for carotenoid conversion are highly derived, the diversity of the clades that possess them suggests that this assumption may need to be revisited with additional taxonomic sampling.
Many spiders show yellow body patches; the yellow patches on orb weavers may function as visual signals for prey attraction (e.g., Leucauge spp. (Tetragnathidae) (Tso et al. 2007), Nephila spp. (Araneidae) (Chuang et al. 2007), and Argiope spp. (Araneidae) (Bush et al. 2008)), crypsis (e.g., Argiope spp. (Hoese et al. 2006)), or aposematism (e.g., Gasteracantha spp. (Araneidae) (Gawryszewski & Motta 2012)). We hypothesize that carotenoid-based yellows could potentially function as honest signals for sexual selection in highly visual spiders like jumping spiders, as carotenoid-based colors do in many birds (MacDougall & Montgomerie 2003) and fishes (Price et al. 2008).
Like melanin, carotenoids have many important non-coloration functions. Carotenoids are found not only in spider chromatophores, but also in hemolymph and silks (Hsiung et al. 2017a). This suggests that carotenoids may have non-coloration functions, such as functioning as antioxidants to mediate oxidative stress, or even olfactory attraction of prey because carotenoids are the precursor to many molecules associated with the scents of flowers, ripe fruits, and the pheromones of Hymenoptera/Lepidoptera (Heath et al. 2012). Future experiments should be devised to test these hypotheses in spiders.
In some cases, when carotenoids are covalently bonded with proteins to form a stable conjugate, i.e., carotenoprotein (Cheesman et al. 1967), the absorption peak could be significantly red-shifted (i.e., more red light than blue is absorbed), resulting in shorter wavelength colors, such as blue (Weesie et al. 1995). No such example has been found in spiders so far.
2.3 Ommochromes.--Ommochromes were identified in spiders forty years ago (Seligy 1972). Ommochromes produce a range of colors including yellow, orange, red, brown and black in spiders (Fig. 1A inset, C) (Seligy 1972). As far as we are aware, all pigmentary red color investigated in spiders is produced by ommochromes (Seligy 1972; Hsiung et al. 2017a). This is likely because spiders may not be able to produce red carotenoids due to the lack of carotenoid conversion enzymes. Recent experimental data support the hypothesis that the ommochrome-based red hourglass marking on the abdomen of black widow spiders is aposematic, but only to birds, not to their insect prey (Brandley et al. 2016). Crab spiders (Thomisidae) are one of the few groups of spiders that can dramatically change their body color, with some species changing from white to bright yellow on different floral backgrounds over several days (Defrize et al. 2010). Crab spiders achieve this feat by controlling the metabolism of ommochromes (Insausti & Casas 2008, 2009), thereby altering the pigment composition of their chromatophores. This process is called morphological color change (in contrast to physiological color change--some orb weavers can change their body coloration rapidly by expanding/contracting the hypodermal guanocytes and/or chromatophores; see section 3.1), and usually takes days to complete, since the process requires synthesis and degradation of pigments on demand. Another ommochrome-based color change mechanism was described in dragonflies, where males change from yellow (oxidized form) to red (reduced form) when mature. This color change is assisted by autonomous modulation of the cytoplasmic condition, which in turn regulates the redox states of ommochrome pigments within the chromatophores (Futahashi et al. 2012). Whether spiders use this mechanism to regulate ommochrome-based body coloration remains to be tested.
Color change in the crab spider Misumena vatia (Clerck, 1757) was long considered a mechanism for camouflage based on human perception (Thery & Casas 2002), but this has proven to be more complex than assumed when considering the perception from ecologically relevant receivers (Defrize et al. 2010). In general, M. vatia is achromatic-cryptic at long distances, but chromatic-detectable at short distances for bees and birds (The Hardy Rand Rittler (HRR) pseudoisochromatic plates used in color blindness tests are examples of achromatic-cryptic but chromatic-detectable stimuli for humans (French et al. 2008)). The spider could also achieve perfect chromatic crypsis at short distance for bees when viewed against specific flower species. But does this mean that M. vatia is indeed under selection by prey for crypsis? Naive bees visit flowers with or without chromatic detectable spiders at the same rate; "experienced" bees that have survived several unsuccessful spider attacks can display increased rates of "false alarm" and/or could leave the patch of flowers altogether, translating to a loss of available prey even for chromatic cryptic spiders (Defrize et al. 2010). In other words, due to the observed prey "training" effect, being chromatic cryptic may even decrease these spiders' foraging efficiency if the spiders do not have 100% capture rate on their first strike (Ings & Chittka 2008). Furthermore, it was shown that naive bumble bees are innately attracted to flowers with a central marking that has higher spectral purity than the petal colors, and flowers with high petal/background color contrast (Lunau et al. 1996). Another example is, instead oftrying to be cryptic, UV reflective crab spiders Thomisus spectabilis Doleschall, 1859) actively choose non-UV reflective surfaces as their hunting sites (Bhaskara et al. 2009), and attract bees with the high UV contrast (Heiling et al. 2005). Hence, we should not always assume crypsis is the function when the colors seem to be matching based on human visual perception.
2.4 Bilins.--Bilins are mostly green, but their color can be shifted to red or blue depending on their chelating metal ions and other conjugates (e.g., proteins or saccharides). Bilin is another class ofpigments described in spiders quite some time ago (Holl & Rudiger 1975). However, little is known about its physiological significance and/or biological functions in spiders. One study in skinks suggested that high concentration of bilin pigments in the circulatory system defends against parasites (Austin & Perkins 2006). Bilin has been found in the hemolymph, interstitial tissues, and yolk of oocytes in spiders (Oxford & Gillespie 1998). Bilin is also thought to cause most non-iridescent green colors ofspiders (Fig. 2A) (Holl 1987), as it does for Lepidoptera (Barbier 1981), Orthoptera, Mantodea (Rudiger et al. 1969), and Diptera (Rudiger & Klose 1970). In addition, non-iridescent green coloration can also be produced by the interaction of pigmentary yellow and structural blue/green in many other animals (especially in vertebrates). It is possible that some spiders produce green using this strategy as well (see 5.1.1).
2.5 Pterins.--Pterins are abundant in many animals (Steffen & McGraw 2007; Wijnen et al. 2007; Johnson & Fuller 2014), and range from white (leucopterin), to yellow (xanthopterin), to red (erythropterin) to the human eye (Wijnen et al. 2007; Wilts et al. 2011). Its high refractive index means that pterin granules scatter light well, similar to melanin granules (i.e., melanosomes). As a result, animals use pterin granules to enhance the brightness of their own pterin colors (Morehouse et al. 2007; Wilts et al. 2017). Pterin pigments have not yet been identified in spiders, however, a genomic study suggests that spiders might be able to synthesize pterins de novo (Croucher et al. 2013). We follow a similar method (tblastn) described in Croucher et al. 2013, and search for genes essential to de novo purine/pterin biosynthesis in the recently published genome of Nephila clavipes (Linnaeus, 1767) (NepCla1.0, online at https://www.ncbi.nlm.nih.gov/assembly/GCA_002102615.1/) using homologous enzyme sequences from D. melanogaster. We find all the essential genes (ade3, Aprt, Prat, bur, ras, Pu, pr), which further suggests that spiders could synthesize pterin de novo. However, we could not verify the presence of pterins in spiders using Raman spectroscopy, possibly because they are chemically Raman-inert molecules (Hsiung et al. 2017a). Surface-enhanced Raman spectroscopy (SERS) or other methods may enable detection of pterins in spiders.
The second color production mechanism involves structures with sub-micrometer size features that are usually made of periodically arranged transparent/translucent materials. Colors produced by this mechanism are often called "structural colors", and are produced by optical processes such as refraction, diffraction, interference, and scattering from the organized materials (Fig. 4). Many examples of structural color exist in nature, both biotic and abiotic, that showcase a full rainbow of colors (Kinoshita 2008; Sun et al. 2013). In particular, most blue color in living organisms is produced by photonic structures instead of pigments. The rarity of blue pigments suggests that they are more difficult to produce/evolve than structures that selectively reflect blue light. (Bagnara et al. 2007; Umbers 2013). It is worth noting that, unlike fluorophores and pigments where each molecule has a characteristic emitting/absorbing spectrum that produces its own specific color dictated by the molecular/chemical structures, photonic structures can, in theory, produce any color within the available irradiation spectrum without changing their chemical/material composition and topology (structural composition). Therefore, the following paragraphs are organized by either their constituent materials or topology rather than color appearances.
3.1 Guanine crystals.--Guanine is a purine that is typically excreted or metabolized immediately after its production. However, in spiders (Oxford 1998), fishes (Levy-Lior et al. 2008, 2010; Gur et al. 2013) and squamates (snakes and lizards) (Kuriyama et al. 2006), guanine is deposited and stored in a crystalline form in vesicles of specialized cells called guanocytes, where the guanine crystals are used as colorants. Although colloquially, the guanine crystal is often referred as a "pigment", like titanium dioxide (Ti[O.sub.2]) particles in white paints, guanine crystals produce color by scattering light, rather than through light absorption. Guanine crystals scatter light efficiently due to their high refractive index ([n.sub.r] -1.83) (Kim 2012). In spiders and fishes, guanine crystals are usually deposited in a variety of orientations in guanocytes (Foelix 2011) (see 3.2), and produce different visual appearances depending on the shapes of the crystals (Fig. 3A, B). While bulky, cube-like guanine crystals scatter light more diffusely and produce matte white (Fig. 3A), thin, plate-like guanine crystals scatter light more specularly (i.e., obey the law of reflection), hence producing a silver, mirror-like appearance (Fig. 3B) (Oxford 1998; Levy-Lior et al. 2010; Gur et al. 2014). Many species of Araneidae, Philodromidae, Tetragnathidae, and Theridiidae can change their body coloration rapidly by changing the arrangement and distribution of guanine granules in the hypodermis through a process called physiological color change (Wunderlin & Kropf 2013).
When guanine crystals are well-organized in a guanocyte, the guanocyte effectively becomes a photonic crystal--a periodic optical structure (Fig. 3C inset; see also section 3.5). Iridophores are cellular vesicles that act as photonic crystals. Many colors can be produced by iridophores through variation in spacing between the scattering elements, in this case the guanine crystals. Guanine crystal based iridophores produce the blue/green hues in many fishes (Hiroshi et al. 1990) and lizards (Kuriyama et al. 2006), and also the dynamic color change in chameleons (Teyssier et al. 2015). So far, no guanine crystal based iridophores have been described in spiders. However, the extremely bright and metallic blue and green opisthosoma patches on a tetragnathid spider--Opadometa sarawakensis Dzulhelmi & Suriyanti, 2015 (Fig. 5) (Dzulhelmi et al. 2015)--may be produced by guanine crystal based iridophores, since they are confined in chromatophore-like compartments in the hypodermis (Fig. 5 inset). Other metallic and iridescent blue/green colorations in spiders known so far result from photonic structures in the exoskeleton (e.g., cuticle or integument setae), rather than iridophores. Future investigation of color production in O. sarawakensis should provide us with a definitive answer for this hypothesis.
3.2 Disordered structures.--Disordered structures are randomly ordered structures that lack both short- and long-range periodicity. A disordered structure can produce white and/or silver by acting as a broadband reflector (wavelength independent scattering); it can also produce blue via Rayleigh scattering (scattering intensity - [[lambda].sup.-4]), such as the blue sky (Strutt 2009), or through the Tyndall effect for colloidal suspensions (Tyndall 1869). However, most biological examples of blues once thought to be produced through incoherent scattering by disordered structures were later falsified, and new data suggested that these blues were instead produced through coherent scattering by quasi-ordered spongy structures (Prum et al. 1998, 2004; Prum & Torres 2003, 2004, 2013) (see section 3.3). Broadband-reflecting disordered structures that produce white/silver are known in white beetle cuticles (Fig. 3D) (Vukusic et al. 2007; Luke et al. 2010; Burresi et al. 2014). Although most spiders produce white/silver with guanocytes that contain disordered guanine crystals, some white/silver setae of spiders are too small to contain guanocytes. Hence, the white/silver color of these setae may be produced by disordered structures made of chitin and air, or by leucopterin pigments that only absorb UV light and scatter all other wavelengths of light. However, these white/silver setae do not fade over time suggesting that their color has structural origins (Oxford 1998).
3.3 Amorphous spongy structures (photonic glasses).--Here, we define amorphous spongy structures (i.e., photonic glasses) as quasi-ordered structures with only short-range order between neighboring elements but not long-range periodicity across distant elements. Amorphous spongy structures scatter light coherently at specific wavelengths depending on their short-range periodicities. Due to the short-range only periodicity, amorphous spongy structures are isotropic to light. As a result, the wavelengths of light scattered by amorphous spongy structures are not angle dependent, and hence they produce non-iridescent structural colors. Theoretically, amorphous spongy structures could produce any color within the visible spectrum (Magkiriadou et al. 2014). For some unknown reasons, amorphous spongy structures are rare in nature, and mostly produce blue hues. The best studied examples are from blue non-iridescent bird feathers (Fig. 3E) (Noh et al. 2010; Saranathan et al. 2012). Two types of amorphous spongy structures are described in bird feathers, the sphere-type (Fig. 3E inset i), and the channel-type (Fig. 3E inset ii) (Saranathan et al. 2012). A sphere-type spongy structure consists of many individual compartments (scatterers) that reside with a continuous matrix made of a different material; while a channel-type spongy structure is a bicontinuous structure of two materials. We recently described similar channel-type amorphous spongy structures in four species of tarantulas (Theraphosidae), including Bumba pulcherrimaklaasi (Schmidt, 1991), Tapinauchenius violaceus (Mello-Leitao, 1930), Chromatopelma cyaneopubescens (Strand, 1907), and Caribena laeta (C.L. Koch, 1842) (Hsiung et al. 2015b). Preliminary data from transmission electron microscopy (TEM) suggest that sphere-type amorphous spongy structures could also be present in spiders (Fig. 6A). Thus, amorphous spongy structures are likely more broadly distributed across animals than previously thought.
Researchers sometimes use terms like "opal" and "inverse-opal" to describe sphere-type photonic structures. Opal structures have sub-micrometer spherical scatterers made of solid materials with refractive indices higher than the air that surrounds them. By contrast, inverse-opal structures have scatterers composed of spherical voids (typically containing air) surrounded by higher refractive index materials. Inverse-opal structures are common in synthetic optical materials, because they require smaller distances between the scatterers due to the matrix's high refractive indices (Johnson et al. 2001; Waterhouse & Waterland 2007). Biogenic inverse-opal photonic glass has previously been described only in blue non-iridescent bird feathers (Noh et al. 2010; Saranathan et al. 2012). However, preliminary data suggest that the non-iridescent blue color in the opisthosoma of the peacock spider Maratus spicatus Otto & Hill, 2012 (Salticidae) may also be produced by specialized setae with inverse-opal photonic glass
structures (Fig. 6A). Further image and numerical analyses are needed to verify the detailed optical principles behind the observed hue and structure. If the analyses support this hypothesis, it would be the first non-feather inverse-opal photonic glass described. This suggests that we may find more novel biogenic photonic structures in the highly visual (potentially with tetrachromatic vision) Australian peacock spiders (Maratus spp.) in the future.
3.4 Multilayer structures.--Multilayer (thin film) structures are likely the most common color production structures in nature, especially in arthropods (Sun et al. 2013). The behavior of light encountering a multilayer structure obeys Snell's law of refraction (Fig. 4A), hence colors produced by multilayer structures can be predicted and simulated closely by the light interference theory (Troparevsky et al. 2010). On the other hand, multilayer structures are also known as Bragg reflectors, since the colors they produce can also be well approximated by the Bragg's law of diffraction (Fig. 4B). Hence, a multilayer structure is technically a one-dimensional (1D) photonic crystal, although it is usually treated as a special case and discussed separately. Bragg reflectors behave like selective mirrors that only reflect certain wavelengths of light and not others, resulting in the observed colorations. Due to light interference, the constructively and destructively interfered wavelengths are determined by the angle dependent optical path lengths, hence the resulting colors are iridescent, and the colors become purer and more intense as the number of layers increases. Iridescence has been proposed to serve many important visual functions (e.g., conspecific recognition, mate choice, crypsis, aposematisms) and non-coloration functions (e.g., thermoregulation, photoprotection, mechanical strengthening, friction reduction, water repellency) (Doucet & Meadows 2009), but may also be a non-adaptive byproduct (Doucet & Meadows 2009; Seago et al. 2009; Barthelat 2010; van der Kooi et al. 2014). Multilayer structures occur in many species of spiders (Fig. 2B, C) (Land et al. 2007; Ingram et al. 2009, 2011; Simonis et al. 2013), and were once thought to be the only structural color production mechanism in tarantulas (Foelix et al. 2013) before amorphous spongy structures were found (Hsiung et al. 2015b).
3.5 Photonic crystals.--The term "photonic crystal" refers to periodic optical structures, and is usually reserved for structures with more than one direction of periodicity (i.e., 2D (Yoshioka & Kinoshita 2002; Trzeciak & Vukusic 2009) or 3D) (Fig. 4B). Depending on the geometry composing a single crystal lattice, 3D photonic crystals can roughly be described as gyroid (Michielsen & Stavenga 2008; Saranathan et al. 2010), cubic close-packed (ccp, i.e., face-centered cubic/fcc), hexagonal close-packed (hcp), and diamond (Galusha et al. 2008) type photonic crystals (Saranathan et al. 2015). Photonic crystal structures are well known in birds (Fig. 3F), butterflies, and beetles. However, photonic crystals have not been described in spiders yet. Preliminary data suggest that the peacock spider Maratus speciosus (O. Pickard-Cambridge, 1874) may have specialized setae with a 2D photonic structure (Fig. 6B) that produce the iridescent blue color on the opisthosoma.
3.6 Diffraction gratings.--Diffraction gratings are structures with parallel ridges or grooves (Fig. 4C), and are seldom used as a major color production element in nature (Kinoshita & Yoshioka 2005), although they are often found in combination with pigments and/or other structural mechanisms to produce complex visual appearances (Parker & Hegedus 2003; Doucet & Meadows 2009). Diffraction gratings can produce intense iridescent effects (Fig. 4C), even more so than what can be achieved by photonic crystals. The end result is a rainbow-like appearance (Seago et al. 2009) similar to that on the back of a compact disk (CD). The rarity of the rainbow-like iridescence in living organisms supports the notion that colors are rarely produced solely by diffraction gratings in these organisms, even though the fossil record suggests that diffraction gratings are one of the most ancient biological photonic structures (Barrows & Bartl 2014). Diffraction grating-like structures have been described in the seed shrimp (Azygocypridina lowryi) (Parker 2002), nacres of mollusks (Shigley et al. 1999; Wong et al. 2004), and in some beetles (Seago et al. 2009), butterflies (Vigneron et al. 2010), wasps (Hinton et al. 1969), snakes (Dhillon et al. 2014) and plants (Whitney et al. 2009). These structures have likely evolved for non-coloration primary functions (van der Kooi et al. 2014), such as mechanical strengthening (Barthelat 2010), water repellency, and friction reduction ( Doucet & Meadows 2009; Seago et al. 2009). Weak iridescence resulting from diffraction grating-like structures in some flowers were hypothesized to function as a visual signal to attract pollinators (Whitney et al. 2009, 2016; Vignolini et al. 2015a, b). However, new research suggests that these structures do not function as diffraction gratings and instead act as quasi-disordered structures that scatter short wavelength "blue light" at specific narrow angles, that guides the pollinators to the stamens and nectar, hence "blue light" instead of iridescence is the salient portion of the visual signal (Moyroud et al. 2017). This concept is similar to the precision approach path indicator (PAPI) systems beside airport runways that aviation engineers designed to assist pilots land their aircrafts during their final approach.
Diffraction grating-like structures have been described optically in some species of jumping spiders (Salticidae), but they usually do not act as primary color producing mechanisms. The first grating-like structure was described on the surface of prosoma cuticle of a Castaneira sp. Keyserling, 1879 (Corinnidae). The cuticle on its own has a multilayer structure that produces green, and the surface "diffraction grating" has a period of ~ 150 nm, which is too small to diffract visible light, and acts as a zero-order grating antireflection mechanism (Parker & Hegedus 2003). Another diffraction grating structure was described on the surface of prosoma cuticle of the jumping spider Cosmophasis thalassina (C.L. Koch, 1846). The cuticle on its own has a "chirped" multilayer structure (i.e., a depth-graded multilayer; see also section 5.4) that acts as a broadband reflector--the reflectance is independent of wavelength across a large electromagnetic range, such as the entire visible spectrum. And the surface grating structure of Cosmophasis thalassina only diffracts blue light at highly oblique angles, due to its short period (~460 nm). As a result, the grating structure of Cosmophasis thalassina does not function as a color production mechanism on its own, but rather as a modifier to remove the blue light from the broadband (white) reflector underneath to produce the final yellow/gold appearance (Parker & Hegedus 2003).
We recently described diffraction grating structures on the rainbow iridescent setae of two species of peacock spiders (M. robinsoni Otto & Hill, 2012 and M. chrysomelas (Simon, 1909)) (Fig. 3G). To the best of our knowledge, these are the first known biological examples of diffraction gratings as the main color production mechanism in a visual signal, especially one used during courtship. Hence, the diffraction gratings on these setae likely evolved under the pressure of sexual selection, and are maximized for their color production ability. Indeed, the periods of these two diffraction gratings are about 500~800 nm, perfect for diffracting visible light. In addition, the gratings and setae are three dimensional with an upward orientation, and thus produce a reversed diffraction order similar to that in the Pierella butterfly (Vigneron et al. 2010). Finally, the special shape of these rainbow setae allow the grating structures to disperse light at a resolution about two times higher than conventional flat 2D diffraction gratings with similar periods (see section 5.3) (Hsiung et al. 2017c). The example from the rainbow peacock spiders shows that diffraction gratings indeed can evolve as a primary color production mechanism under selection, instead of a coincidental or epiphenomenon trait.
Some organisms can produce colors by actively emitting light. However, the intensity of the biologically emitted light is usually very weak relative to other sources of illumination (e.g., sunlight), and can only be observed when certain conditions are met (e.g., in a dark environment). Therefore, this mechanism is typically only found in caves and the deep sea, or in nocturnal organisms.
Fluorescence occurs when molecules called fluorophores absorb shorter wavelengths of light and almost immediately release most of the absorbed energy by emitting light at longer, lower energy, wavelengths. Therefore, no light is emitted when the shorter wavelengths of light (e.g., UV) are absent. Fluorescence was once thought to be rare in organisms, but we now know that it is widespread among marine organisms, including corals (Alieva et al. 2008), sea anemones (Tu et al. 2003), jellyfish (Zimmer 2009), and fishes (Sparks et al. 2014). Fluorescence also occurs in plants (Lang et al. 1991; Gandia-Herrero et al. 2005; Kurup et al. 2013) and a handful of terrestrial animals (Arnold et al. 2002; Welch et al. 2012), including most scorpions (Gaffin et al. 2012, but see Lourenco 2012), many spiders (Andrews et al. 2007), and even frogs (Taboada et al. 2017). Fluorescence has been suggested to serve functions like photoprotection (Salih et al. 2000), prey attraction (Kurup et al. 2013), mate choice (Arnold et al. 2002; Lim et al. 2007), and even assistance in vision (e.g., to increase contrast (Meadows et al. 2014) or light perception (Gaffin et al. 2012)). Although Andrews et al. (2007) argued that that fluorescence in scorpions is likely a by-product or epiphenomenon that serves no important biological function, Gaffin et al. (2012) provided convincing evidence that fluorescence in scorpions plays an active role in light detection. In spiders, the fluorophores are usually diffusely distributed in the hemolymph, and sometimes concentrated in the cuticle or setae (Andrews et al. 2007). Fluorescence in spiders is likely functional since the fluorophores often form particular patterns due to cuticle and/or setae sequestration and new fluorophores continuously evolved during spider diversification, indicating that fluorescence is a labile trait that has evolved multiple times in spiders (Andrews et al. 2007). Indeed, it has been demonstrated that fluorescence is an important visual signal during mate choice in the jumping spider Cosmophasis umbratica Simon, 1903 (Lim et al. 2007). It is also worth noting that this fluorescent signal is functional during daylight, as it enhances the perceived colors a la DayGlo[TM] (daylight fluorescent pigments, Day-Glo Color Corp., Cleveland, OH, USA). This is in contrast to the general notion that colors in nature produced by light emission can only be observed in dark environments due to low quantum yields. It subsequently suggests the fluorophores that female C. umbratica produced might have exceptional quantum yield compared to most biological fluorophores in nature. It would therefore be interesting to study the chemical/genetic nature of this specific fluorophore and its evolution in the future. Whether spider fluorescence also functions as a visual cue for prey attraction remains to be tested (Thorp et al. 1975; Kurup et al. 2013, but see Iriel & Lagorio 2010). The chemistry of spider fluorophores is also largely unknown and awaits further investigation.
Bioluminescence refers to light emission due to chemical/enzymatic reactions, and was once thought to occur only rarely (Herring 1987). In contrast to fluorescence, bioluminescence is the only known mechanism in organisms that can emit light without any external source of irradiation. Currently, there is no known example of bioluminescence in spiders.
5. COLOR BY INTERACTION OF MULTIPLE ELEMENTS
Pigments, photonic structures, and fluorescence are historically treated as independent mechanisms of color production. Researchers tend to investigate each mechanism in isolation. However, more and more evidence suggests that different color production elements interact to produce the final visual appearances (Shawkey & D'Alba 2017). Known examples of these interactions are summarized and discussed below.
5.1 Pigmentary--structural color interaction.--5.1.1 Color mixing: The interaction between pigments and structural colors can be simple color mixing, of which the most prominent natural example is non-iridescent green. Many animals produce non-iridescent green by mixing yellow pigments with blue or blue-green structural colors (Bagnara et al. 2007; D'Alba et al. 2012). Typically, the yellow pigmentary chromatophores are overlaid on top of the blue structural color producing iridophores (Saenko et al. 2013). It is possible that spiders could produce green through pigmentary-structural color mixing because spiders have the necessary pigmentary and structural palettes to do so. However, no such example has been described in spiders yet. Here, we propose that some Leucauge spp. (Fig. 2D) and other similar spiders produce green body patches by a layer of yellow carotenoid chromatophores with a layer of blue guanine iridophores underneath (Fig. 2D inset C+I). This hypothesis can be tested by examining the green body patches further, using electron microscopy to see if periodically organized guanine crystals with the right spacing that produces blue/blue-green colors are present in these areas.
5.1.2 Light absorbing backgrounds: Dark pigments (usually melanins) can make structural colors appear more saturated and conspicuous by absorbing randomly scattered light (Kinoshita et al. 2002; Shawkey & Hill 2006). This effect results in the bright and flashy feathers of hummingbirds and can be achieved in several ways. First, pigments can be deposited inside vesicles or granules in chromatophores arranged randomly beneath the photonic structures, as in birds (Shawkey & Hill 2006) and peacock spiders (Hsiung et al. 2017a). Alternately, pigments can be diffusely distributed and form a homogeneous layer beneath the photonic structures, as in many butterfly wing scales (Kemp 2002) and the highly iridescent hairs from the chelicerae of the tarantula Ephebopus cyanognathus West & Marshall, 2000 (Foelix et al. 2013). The pigment layers can be observed in transmission electron microscopy (TEM) as more electron-dense (darker) material in the micrographs. Moreover, pigments can be mixed homogeneously with the building materials (e.g., chitin) of the photonic structures, as shown in examples from some butterfly wing scales (Vukusic et al. 2004). Other than peacock spiders, this type of interaction can also be seen in blue tarantulas, where the structural blue setae are interlaced with pigmentary black setae to increase the saturation of the blue color.
Dark, black colorations are often attributed solely to pigments with strong absorbance, such as melanins. However, pigments alone have their limitations. A portion of light will inevitably be reflected when hitting a highly absorbent but smooth material, due to the sudden refractive index difference at the interface that causes a glossy sheen appearance. To overcome this limitation, microscopic surface structures are needed to produce an appearance that is less reflective and darker than achieved with pigments alone. This kind of pigmentary--structural interaction is dubbed a "structurally assisted black." Structurally assisted black can result from anti-reflection structures, such as GRIN (graded refractive index) (Eliason & Shawkey 2014) and the moth eye structure (Wilson & Hutley 1982). In addition, three other examples of structurally assisted black have been described in butterflies (Vukusic et al. 2004), snakes (Spinner et al. 2013), and birds-of-paradise (McCoy et al. 2018). Interestingly, although not thoroughly studied, the black setae of many species of peacock spiders show similar optical properties and microstructures that resemble the structurally assisted black barbules of birds-of-paradise but at an even smaller length scale (Fig. 7).
5.1.3 Light reflecting backgrounds: Generally, pigments that assist in production ofstructural colors are located in the inner layers beneath the photonic structures that are proximal to the skin surface or cortex. This kind ofspatial relationship enables the pigments to absorb randomly scattered light and minimize the background noise. However, the lighter yellow and red pigments alone do not have enough "tint strength" to be perceived on their own against dark backgrounds and instead need strongly reflecting backgrounds from which they can absorb light (Shawkey & Hill 2005). This kind ofinteraction is nearly ubiquitous in paints. Titanium dioxide (Ti[O.sub.2]) particles are used as a basal colorant in most paints while additional pigments are added to produce the colors (Stallknecht 2013). TiO2 scatters light across the entire visible spectrum, producing a white appearance. However, when TiO2 acts in concert with the pigments in paints, it increases the brightness of the pigments, and masks the surface beneath it, so that the color of the paints can be perceived faithfully on any kind of surface (Reck & Seymour 2002). In living organisms, guanine crystals act analogously to TiO2 in paints. Guanine crystals are deposited in guanocytes of spiders (Oxford 1998; Levy-Lior et al. 2010), and iridophores of some squamates (Saenko et al. 2013), acting as light reflecting backgrounds to the pigment layers on top of them, thereby increasing the brightness of the pigmentary color and making the colors more conspicuous. This kind of interaction is common for production of yellow (Fig. 2D inset C+G) and red (Fig. 1A inset) in spiders as well. In these cases, the photonic structures are buried underneath the pigment-containing chromato-phores. Guanine is a metabolic intermediate from nutrient digestion. Storing guanine crystals inside the bodies may cost more energy for animals compared to excreting it (Oxford 1998). So why are animals storing guanine inside their body and using it as a color production mechanism if it is costly? It was suggested that lizards having brighter body coloration as a result of guanine crystals have higher reproduction success (LeBas & Marshall 2000; Moln^r et al. 2012), making it a worthwhile investment. One study also suggests that conspicuous patterns produced by guanine crystals in orb-weaving spiders increases foraging success by attracting more prey to the web (Blamires et al. 2014). However, there may be other non-signaling functions for guanine crystals, for example thermoregulation, or UV-protection.
5.2 Interactions between structural elements across different spatial scales.--This type of interaction is purely structural, occurring between nano-scale photonic structures and larger micro- and/or meso-scale structures (particularly due to their shapes), together producing the final, macro-scale visual appearances.
Photonic structures may gain different optical properties from different geometrical features, such as curvature, surface roughness, or hierarchy. The most well-known example is probably the green wing scales of the male Papilio palinurus butterfly, where the green color is a mixture of yellow and blue produced by the nano-scale multilayer structure, and the micro-scale concave shape of a single butterfly wing scale (Fig. 8A) (Vukusic et al. 2000). Due to the concave curvature on the surface of the wing scale, when light comes from the same incident direction, blue is reflected back around the circumference, and yellow is reflected at the center of the concavity by the curved multilayer structure. The final macroscopic appearance of green is produced by color mixing. Some other examples found in birds and butterflies showed that iridescence produced by multilayer interference can be enhanced by arranging the multilayers into different shapes and orientations (Vukusic et al. 2001; Stavenga et al. 2011; Wilts et al. 2014). However, the resulting iridescence usually shifts between only a few discrete (i.e., not neighboring) hues and do not cover all colors in the visible spectrum (flashing/sparkling effects).
Since natural structures are often hierarchical across several orders of spatial scales, this kind of interaction could be widespread in nature (Bae et al. 2014). Indeed, blue structurally colored setae from some tarantulas, such as Poecilotheria metallica Pocock, 1899 (Foelix et al. 2012) and Lampropelma violaceopes Abraham, 1924, show multilayer structures with hierarchical cylindrical groove-like configurations along their length (Fig. 8B). Using finite element analysis (FEA) and nano 3D-prototyping, we determined that this hierarchical geometry with its high degree of rotational symmetry (flower-like shape) almost entirely eliminates the iridescence produced by the multilayer structure, producing highly consistent blue color from all viewing angles (Hsiung et al. 2017b). Another example of this type of interaction is the rainbow iridescent setae from the peacock spiders M. robinsoni and M. chrysomelas. The rainbow setae combine nanoscale 2D diffraction grating structures with microscale 3D convex curvature (Fig. 8C), enabling the setae to separate different wavelengths of light at a higher resolving power than the conventional, flat diffraction grating (Hsiung et al. 2017c). Above research on spiders overturns the conventional notion in optics that periodic photonic structures are definitely iridescent, and rainbow iridescence produced by diffraction gratings cannot be further enhanced by interacting with microscopic shapes. This suggests that many more surprising and complex visual effects produced via "nano-micro" interactions may be waiting to be discovered in nature.
The electric blue tarantula--Chilobrachys sp. is marketed as the most vibrant iridescent blue tarantula in the pet trade. The iridescence of the setae of Chilobrachys Karsch, 1892 has its origin in the asymmetric hierarchical configuration of the setae (Fig. 8D). And the setae are highly vibrant because their multilayer structure is composed of a larger number of layers than found in typical blue tarantulas. Whether or not the flattened shape of the setae of Chilobrachys alters the optics of the multilayer structure significantly as it does for Poecilotheria Simon, 1885 and Lampropelma Simon, 1892 remains to be determined.
5.3 Interactions between order and randomness.--The last type of interaction is again purely structural. It is the interplay between order and disorder, and one example is the irregular multilayer structure when homogenous thin films with varying thickness are stacked together with no particular arrangements (i.e., randomly), combining order and randomness. A type of irregular multilayer structure can be observed in the Morpho blue butterflies (Fig. 3H). The blue is produced by Christmas tree surface structures with an ordered spacing between each branch. However, the height of neighboring Christmas tree structures on the scales are randomly offset (Fig. 3H inset). This irregularity decreases the angle dependence of the structural blue produced by the Christmas tree structures, so that the bright metallic blue from the Morpho butterfly can be seen from wider angles than colors produced by perfectly periodic Christmas tree structures (Saito et al. 2011; Siddique et al. 2013).
Theoretically, three types of multilayer structures can function as broadband reflectors (Parker et al. 1998); all of them involve some degrees of irregularity: 1. overlapped--this type of multilayer is composed of many regular multilayer structures, each with a different periodicity that reflects different wavelengths of light, which are stacked together to form a supra-multilayer structure (Fig. 9A). 2. chirped--this type of multilayer has no consistent spacing between two closest neighboring layers. Instead, the layers are arranged so that the spacing between neighboring layers increases/decreases gradually (Fig. 9B). 3. chaotic--the arrangement of this type of multilayer is completely random. However, a chaotic multilayer structure still retains a minimum order in that all layers are parallel to each other (Fig. 9C) (Parker et al. 1998). The chirped multilayers, but not overlapped multilayers, are commonly found in arthropods (spiders included), potentially due to the process of how cuticle is formed.
Our understanding of how color is produced in spiders has advanced significantly during the past decades by incorporating new research techniques and workflows into this long-established field, and because of broader taxonomic sampling across major groups of spiders. Spiders have a much larger and more complex toolbox to produce colors at their disposal than previously thought, although much of spider diversity still remains unexplored. Color production in spiders is therefore likely as elaborate and diverse as in other colorful groups of organisms like birds and butterflies.
Knowledge about how color is produced in other organisms can inform and identify gaps in our knowledge of spiders and vice versa. For example, the novel photonic structure--shape interactions found in blue tarantulas and peacock spiders reveal mechanisms in spiders that are not yet described in other organisms. And modulation of pigmentary colors through changes in pH, redox conditions, ion chelation, and/or covalent conjugation is well-described in other organisms but is yet to be investigated in spiders. Current research on spider coloration is limited by its narrow taxonomic scope. Studies tend to focus on jumping spiders, tarantulas, orb weavers, and crab spiders. Novel color production mechanisms in spiders will continue to be discovered, as more and more spider species are described and studied in detail, for example: Opadometa sarawakensis with bright yellow/red and metallic blue markings mentioned earlier, and/or other equally colorful but less studied spiders, such as lynx (Oxyopidae spp.) and ladybird (Eresus spp., Eresidae) spiders.
A color is rarely produced by just a single mechanism, and instead usually results from interactions between two or more mechanisms. In addition to simple color mixing that modulates hue, these multi-mechanism interactions can also modulate a myriad of other optical properties, such as iridescence, gloss, brightness, and saturation. Many of these properties could reflect individual spider condition, and hence potentially be used as honest signals for communications. Understanding how colors are produced is just one piece of the puzzle required to fully decipher the function of colors. To test hypotheses about the functions of color, one also needs to consider the evolutionary ecology and sensory physiology of the intended receivers, and potential non-visual functions of the coloration.
Understanding the color production mechanisms in spiders will also contribute to the advancement of our knowledge about the evolution, ecology, adaptation, and functions of these traits. Therefore, it is important to continue moving this field forward through broader phylogenetic sampling and more rigorous description of mechanisms.
We thank all the photographers, authors and publishers who granted us the permission to use their images in this manuscript. This research was funded by the National Science Foundation (IOS-1257809, T.A.B.), Air Force Office of Scientific Research (FA9550-16-1-0331 and FA9550-18-1-0477, M.D.S.), Human Frontier Science Program (RGY-0083, M.D.S.), Fonds Wetenschappelijk Onderzoek
(G007177N, M.D.S.) and The University of Akron Biomimicry Research and Innovation Center (B.-K.H.). B.-K.H. is supported by The Sherwin-Williams Company under a Biomimicry Fellowship.
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Bor-Kai Hsiung (1,2), Matthew D. Shawkey (1,3) and Todd A. Blackledge (1): (1) Department of Biology and Integrated Bioscience Program, The University of Akron, Akron, OH 44325-3908, USA; E-mail: firstname.lastname@example.org; (2) current address: Scripps Institution of Oceanography (SIO), University of California, San Diego, La Jolla, CA 92093, USA; (3) Biology Department, Evolution and Optics of Nanostructures Group, Ghent University, Ledeganckstraat 35, 9000 Ghent, Belgium
Manuscript received 2 April 2018, revised 25 January 2019.
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|Author:||Hsiung, Bor-Kai; Shawkey, Matthew D.; Blackledge, Todd A.|
|Publication:||The Journal of Arachnology|
|Date:||May 1, 2019|
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