Reversible colour change in Arthropoda

The mechanisms and functions of reversible colour change in arthropods are highly diverse despite, or perhaps due to, the presence of an exoskeleton. Physiological colour changes, which have been recorded in 90 arthropod species, are rapid and are the result of changes in the positioning of microstructures or pigments, or in the refractive index of layers in the integument. By contrast, morphological colour changes, documented in 31 species, involve the anabolism or catabolism of components (e.g. pigments) directly related to the observable colour. In this review we highlight the diversity of mechanisms by which reversible colour change occurs and the evolutionary context and diversity of arthropod taxa in which it has been observed. Further, we discuss the functions of reversible colour change so far proposed, review the limited behavioural and ecological data, and argue that the field requires phylogenetically controlled approaches to understanding the evolution of reversible colour change. Finally, we encourage biologists to explore new model systems for colour change and to engage scientists from other disciplines; continued cross‐disciplinary collaboration is the most promising approach to this nexus of biology, physics, and chemistry.     

浅谈色彩在昆虫绘画中的应用

尝试以彩色绘画的方式表现昆虫的体貌特征,应先认识色彩,了解色彩的特性,以色彩变化的基本规律去观察昆虫体色的微妙变化,分析、找出昆虫体壁每一部分的色彩倾向。绘画时,只有掌握并运用色彩的特性及色彩的对比关系,在平面的纸张上才能表现出昆虫的立体效果。     

Physiological control of the chromatophores of Austrolestes annulosus (Odonata)

The chromatophore-containing integument of Austrolestes annulosus always changes from a dark to a blue colour phase in vitro and therefore functions independently of a central control mechanism. In isolated abdominal segments, the reverse colour change occurs independently of the presence of central nervous system. The amount of change decreases with the size of the piece of integument; it varies over different parts of the body of the same intact insect, and it varies both in vitro and in vivo with time of day.A variety of experiments, involving ligation of abdominal segments and ablation of their ganglia, show that the terminal ganglion is primarily responsible for the release of a darkening factor which migrates in an anterior direction. Other ventral ganglia have a similar function but are of less importance.Transplants of terminal ganglia and injection of their extracts fail to restore capacity for colour change in ligature-isolated segments which have had their own ganglia removed. These findings, supported by histological observations, suggest that the darkening factor is a neurosecretion.     

Structure and colour of the integument of the European eel Anguilla anguilla (L.)

The structure of the integument of 26 wild and nine artificially matured female Anguilla anguilla , and 30 sexually immature eels maintained in controlled lighting, was investigated. Melanophore densities varied in a way unrelated to maturity while xanthophores were progressively lost from lower levels in the skin. Reflecting layers made up of the purines, guanine and hypoxanthine were associated with chromatophore layers. Purine concentrations (as a percentage of total skin dry weight) decreased with maturity but a reorganization of the reflecting elements occurred. Colour changes associated with maturation were due to the redistribution of purines. Spectral and angular reflectance measurements indicate that the integument has camouflage value and colour changes can be related to the change in habitat occurring with migration. The usefulness of colour as an index of sexual maturity is discussed.     

Garotenoids and colouration of poplar hawkmoth caterpillars (Laothoe populi)

Carotcnoids and chlorophylls a and b were extracted from final instar caterpillars of the poplar hawkmoth ( Laothoe populi ) and the eyed hawkmoth ( Smerinthus ocellata ), as well as from their food plants. Both species of caterpillar absorb the two chlorophylls and the carotenoids lutein, cis -lutein and β-carotene in the gut and deposit lutein and cis -lutein in the integument. It is the lutein, together with pterobilin, that is largely responsible for the colour of the insect: yellow-green poplar hawkmoth caterpillars have more lutein in the integument than dull green ones which in turn have more than white ones. Yellow-green and dull green caterpillars both sequester lutein and cis -lutein in the gut wall, but the yellow-greens translocate more of these pigments to the integument than the dull greens. The white caterpillars absorb very little lutein and cis -lutein into the gut, and so they have much less also in the integument. The mechanism by which the reflected light perceived by the caterpillar is translated into differential absorption of pigment by the gut and deposition in the integument is not known.     

Nuclear and mitochondrial data reveal different evolutionary processes in the Lake Tanganyika cichlid genus <Emphasis Type="Italic">Tropheus</Emphasis>

Background  

Cichlid fishes are notorious for their wealth of intra- and interspecific colour pattern diversity. In Lake Tanganyika, the endemic genus Tropheus represents the most impressive example for geographic variation in the pattern and hue of integument colouration, but the taxonomy of the over 100 mostly allopatric colour morphs remains to a large degree unresolved. Previous studies of mitochondrial DNA sequence data revealed polyphyly of the six nominally described species and complex phylogeographic patterns influenced by lake level fluctuations and population admixture, and suggested the parallel evolution of similar colour patterns in divergent evolutionary lineages. A gene tree of a rapidly radiating group may be subject to incomplete and stochastic lineage sorting, and to overcome this problem we used multi-locus, nuclear AFLP data in comparison with mtDNA sequences to study diversification, migration and introgression in Tropheus colour morphs in Lake Tanganyika.     

Iridescent colour production in hairs of blind golden moles (Chrysochloridae)

Relative to other metazoans, the mammalian integument is thought to be limited in colour. In particular, while iridescence is widespread among birds and arthropods, it has only rarely been reported in mammals. Here, we examine the colour, morphology and optical mechanisms in hairs from four species of golden mole (Mammalia: Chrysochloridae) that are characterized by sheens ranging from purple to green. Microspectrophotometry reveals that this colour is weak and variable. Iridescent hairs are flattened and have highly reduced cuticular scales, providing a broad and smooth surface for light reflection. These scales form multiple layers of light and dark materials of consistent thickness, strikingly similar to those in the elytra of iridescent beetles. Optical modelling suggests that the multi-layers produce colour through thin-film interference, and that the sensitivity of this mechanism to slight changes in layer thickness and number explains colour variability. While coloured integumentary structures are typically thought to evolve as sexual ornaments, the blindness of golden moles suggests that the colour may be an epiphenomenon resulting from evolution via other selective factors, including the ability to move and keep clean in dirt and sand.     

The density of odontocete integument depends on blubber lipid composition and temperature

Cetacean integument serves many functional roles, including contribution to whole body buoyancy. The blubber of the integument of different cetacean species contains varying concentrations of triacylglycerols (TAG) and wax esters (WE); generally, these lipid classes have different densities. Integument can also experience a wide range of temperatures during a dive, so its density may change with depth. The goals of this study were to measure integument density and isolated blubber lipid density in three deep‐diving odontocete species (n = 3–4)—short‐finned pilot whales (Globicephala macrorhynchus), pygmy sperm whales (Kogia breviceps), and Gervais' beaked whales (Mesoplodon europeaus)—at different temperatures (6°C–35°C), and to relate these densities to lipid content and composition. Kogia and Mesoplodon integument and isolated lipids had high WE content (78.7–99.5 wt%) and were less dense (by 1.7%–9.3%) than those of Globicephala, which were composed predominately of TAG. Generally, densities increased as temperature decreased. Changes in integument densities mirrored those of isolated lipid densities, suggesting that blubber lipids are largely responsible for the buoyant properties of cetacean integument. These data demonstrate that the contribution of the integument to whole body density depends on lipid class and temperature, and therefore may provide useful, species‐specific correction factors for diving energetics models.     

Phenotypic plasticity in hoverflies: the relationship between colour pattern and season in Episyrphus balteatus and other Syrphidae

1. The abdominal colour patterns of some multivoltine species of hoverfly are phenotypically plastic and change through the flying season.
2. It was predicted how the abdominal colour pattern of one species, Episyrphus balteatus , should change in the field with season based on a hypothesis that the pattern influences the thermoregulatory capabilities of the animal. The colour patterns were quantified using image analysis. The observed changes in the colour pattern through the year supported the thermoregulation hypothesis.
3. A further three Metasyrphus species were analysed similarly to allow a comparative study of the forms of the plasticities of the above four species and four Eristalis species from a previous study.
4. Whilst it was clear that the abdominal colour patterns of many of the species were plastic, it was also apparent that not all species used the same developmental pathway to control the seasonal colour pattern changes. This suggests convergent evolution towards a general type of plasticity and that abdominal colour pattern plasticity in hoverflies is functional.     

The effect of skin reflectance on thermal traits in a small heliothermic ectotherm

Variation in colour patterning is prevalent among and within species. A number of theories have been proposed in explaining its evolution. Because solar radiation interacts with the pigmentation of the integument causing light to either be reflected or absorbed into the body, thermoregulation has been considered to be a primary selective agent, particularly among ectotherms. Accordingly, the colour-mediated thermoregulatory hypothesis states that darker individuals will heat faster and reach higher thermal equilibria while paler individuals will have the opposite traits. It was further predicted that dark colouration would promote slower cooling rates and higher thermal performance temperatures. To test these hypotheses we quantified the reflectance, selected body temperatures, performance optima, as well as heating and cooling rates of an ectothermic vertebrate, Lampropholis delicata. Our results indicated that colour had no influence on thermal physiology, as all thermal traits were uncorrelated with reflectance. We suggest that crypsis may instead be the stronger selective agent as it may have a more direct impact on fitness. Our study has improved our knowledge of the functional differences among individuals with different colour patterns, and the evolutionary significance of morphological variation within species.     

Ovular development and morphology in some magnoliaceae species

Floral phenology and ovular development ofLiriodendron tulipifera are described. The ovule primordia are initiated in December, followed by prominent development in March, and the ovules are mature in May. The inner integument is formed as an annular rim on the incurving ovule primordia, but the outer integument develops as a semi-annular rim interrupted on the concave side of the funicle. Later, an outgrowth, which is interpreted here as an obturator, arises on the concave side of the funicle. The funicular outgrowth arises far from the inner integument, while the outer integument is close to the inner. The outer integument and the funicular outgrowth together form an envelope complex. Later the outer integument produces two distal lobes, which disappear at maturity. Mature ovules of the threeMagnolia species examined have similar lobes. It is suggested that the hood-shaped outer integument is primitive in angiosperms.     

Colour change and camouflage in the horned ghost crab Ocypode ceratophthalmus

Species that change colour present an ideal opportunity to study the control and tuning of camouflage with regards to the background. However, most research on colour‐pattern change and camouflage has been undertaken with species that rapidly alter appearance (in seconds), despite the fact that most species change appearance over longer time periods (e.g. minutes, hours, or days). We investigated whether individuals of the horned ghost crab (Ocypode ceratophthalmus) from Singapore can change colour, when this occurs, and how it influences camouflage. Individuals showed a clear daily rhythm of colour change, becoming lighter during the day and darker at night, and this significantly improved their camouflage to the sand substrate upon which they live. Individuals did not change colour when put into dark conditions, but they did become brighter when placed on a white versus a black substrate. Our findings show that ghost crabs have a circadian rhythm of colour change mediating camouflage, which is fine‐tuned by adaptation to the background brightness. These types of colour change can enable individuals to achieve effective camouflage under a range of environmental conditions, substrates, and time periods, and may be widespread in other species. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 257–270.     

Colour‐variable birds have broader ranges,wider niches and are less likely to be threatened

Coloration fulfils a variety of adaptive functions in animals. Colour variability, both between and within species, can be caused by different colours being favoured for different functions and in different environments. Thus, species with highly variable coloration may have greater potential to persist in new and changing environments. As a consequence, such colour‐variable species may be more able to adapt, colonize new areas and niches, occupy larger ranges, speciate more readily and in general be less vulnerable to environmental change and extinction. These predictions have been supported by comparative analyses on amphibians and reptiles. However, as coloration in ectotherms plays a key role in thermoregulation, it is unclear whether these results can be generalized to endotherms, such as birds and mammals. Here, we test the hypothesis that more colour‐variable endotherms occupy larger ranges/niches and are less vulnerable to the threat of extinction by focussing on colour variation in Australian parrots and passerine birds. As predicted, colour variability was correlated with range size (parrots and passerines) and niche breadth (dietary heterogeneity, parrots only). These relationships support the predicted link between colour variability and adaptability, whereby range size and niche breadth may be a cause of colour variability or vice versa. Irrespective, and as predicted, colour variability was lower in threatened species, even after statistically controlling for other confounding variables. Hence, our study supports the hypothesis that colour‐variable species in general are more resilient to environmental change.     

Body shape variation and colour change during growth in a protogynous fish

Protogynous sequential hermaphroditism is very common in marine fish. Despite a large number of studies on various aspects of sequential hermaphroditism in fish, the relationship between body shape and colour during growth in dichromatic species has not been assessed. Using geometric morphometrics, the present study explores the relationship between growth, body shape and colouration in Coris julis (L. 1758), a small protogynous labrid species with distinct colour phases. Results show that body shape change during growth is independent of change in colour phase, a result which can be explained by the biology of the species and by the social control of sex change. Also, during growth the body grows deeper and the head has a steeper profile. It is hypothesized that a deeper body and a steeper profile might have a function in agonistic interactions between terminal phase males and that the marked chromatic difference between colour phases allows the lack of strict interdependence of body shape and colour during growth.     

Morphological and ontogenetic studies on southern African podocarps. Initiation of the seed scale complex and early development of integument, nucellus and epimatium

STOFFBERG, E., 1991. Morphological and ontogenetic studies on southern African podocarps. Initiation of the seed scale complex and early development of integument, nucellus and epimatium. The primordium of the seed scale complex (ssc) (ovule with epimatium) is initiated in the axil of the first or second cone bracts (prophylls) as a dome shaped structure consisting of a group of uniform, meristematic cells. A distinct protodermal layer develops. The nucellus is a dome on the ventral side of the ssc primordium. In the species of section Podocarpus the integument is initiated as a circular ridge around the nucellus, while in P.falcatus two protrusions on the anterior and posterior sides of the nucellus are the first indications of integumentary differentiation. The integument of all species studied is of subdermal origin. The epimatium (sensu stricto) is initiated after the integument, is of subdermal origin and forms a hood around the developing ovule. Considering research results, together with related literature, it is concluded that the integument of gymnosperms may be homologous with the outer integument of a bitegmic angiospermous ovule, that the position of integumentary initiation may be specific for certain taxa and that there seems to be no constant sequence of emergence of ovular envelopes in gymnosperms.     

Rockpool Gobies Change Colour for Camouflage

Camouflage is found in a wide range of species living in numerous habitat types, offering protection from visually guided predators. This includes many species from the intertidal zone, which must cope with background types diverse in appearance and with multiple predator groups foraging at high and low tide. Many animals are capable of either relatively slow (hours, days, weeks) or rapid (seconds and minutes) colour change in order to better resemble the background against which they are found, but most work has been restricted to a few species or taxa. It is often suggested that many small intertidal fish are capable of colour change for camouflage, yet little experimental work has addressed this. Here, we test rock gobies (Gobius paganellus) for colour change abilities, and whether they can tune their appearance to match the background. In two experiments, we place gobies on backgrounds of different brightness (black or white), and of different colours (red and blue) and use digital image analysis and modelling of predator (avian) vision to quantify colour and luminance (perceived lightness) changes and camouflage. We find that gobies are capable of rapid colour change (occurring within one minute), and that they can change their luminance on lighter or darker backgrounds. When presented on backgrounds of different colours, gobies also change their colour (hue and saturation) while keeping luminance the same. These changes lead to predicted improvements in camouflage match to the background. Our study shows that small rockpool fish are capable of rapid visual change for concealment, and that this may be an important mechanism in many species to avoid predation, especially in complex heterogeneous environments.     

Die Redoxpigmente von Carausius morosus und ihre Bedeutung für den morphologischen Farbwechsel

Summary From the epidermis of Carausius morosus two ommochromes were isolated, and identified by various means as Xanthommatine and Ommine. Their amount was determined by photometry for animals of different colour.Morphological colour change results mainly from changes in ommochrome content.If the lower part of their compound eyes is blackened, green specimens become brown by an increase of ommochrome production.This colour change can be evoked within a single larval instar.It can also be evoked in adult specimens, although to a small degree only.Dark specimens with unblinded eyes become paler under normal illumination in consequence of an increase of bright pigments and of the increase in bodysize, while the amount of ommochrome increases only very slightly.A decrease of ommochrome content or a loss of ommochrome by faeces or offshed cuticles was never observed.At high temperature (28° C) both, ommochrome production in the epidermis and melanin formation in the cuticle are increased.Implantation of supernumerous Corpora allata causes the ommochrome content to increase. After extirpation of the Corpora allata no decrease of ommochrome content is found but the green pigment, insectoverdin vanishes. Apparently in Carausius ommochrome may deposited but is never removed from the integument, which may explain the similar coloration after both experiments.     

Ontogenetic colour change signals sexual maturity in a non-territorial damselfly

Conspicuous colouration increases male reproductive success through female preferences and/or male–male competition. Despite the advantages of conspicuous colouration, inconspicuous male morphs can exist simultaneously in a population due to genetic diversity, condition dependence or developmental constraints. We are interested in explaining the male dichromatism in Xanthagrion erythroneurum damselflies. We reared these damselflies in outdoor insectaries under natural conditions and showed that this species undergoes ontogenetic colour changes. The younger males are yellow and change colour to red 6–7 days after their emergence. We took red and yellow male reflectance spectra and found that red males are brighter than yellow males. Next, we aimed to determine whether ontogenetic colour change signals sexual maturity with field observations and laboratory experiments. Our field observational data showed that red males are in higher abundance in the breeding territory, and they have a higher mating frequency than yellow males. We confirmed these field observations by enclosing a red and a yellow male with two females and found that yellow males do not mate in presence of red males. To determine whether colour change signals sexual maturity, we measured mating success of males before and after colour changes by enclosing a single male at different age (day 3-day 7) and colour (yellow, intermediate and red) with a single female in a mating cage. Males did not mate when yellow but the same male mated after it changed colour to red, suggesting the ontogenetic colour change signals sexual maturity in this species. Our study shows that male dichromatism can be age-dependent and ontogenetic colour change can signal age and sexual readiness in non-territorial insects.     

Colour change ability and its effect on prey capture success in female Misumenoides formosipes crab spiders

1. Changing between white and yellow body colour in certain crab spider species has been interpreted as an adaptation for matching the background colour where they hunt and thereby remaining cryptic to prey and/or their own predators. The potential costs and benefits of colour change in female Misumenoides formosipes Walckenaer were investigated via assessment of prey opportunities and capture success, in conjunction with the tendency for and rate of colour change on different backgrounds. 2. It was tested whether being matched or mismatched to their background affected foraging by moving females between white and yellow inflorescences. Female colour was quantified in digital photos using the Lab colour space component of Adobe photoshop , providing the first empirical assessment of the rate of colour change for a crab spider species. 3. Insect visits (potential prey) on inflorescences with and without spiders and prey capture success with females matched and mismatched to their background were quantified. 4. Yellow females abandoned white inflorescences, whereas white females remained on and underwent colour change on yellow inflorescences. This difference supported the notion that the costs of colour change differ depending on the starting colour. Female departures from white flowers were apparently not due to a lack of insect visitation, as white inflorescences had higher visitation rates than did yellow inflorescences, even in the presence of spiders. 5. An increase in the prey capture success of females who transitioned from white to yellow body colour on a yellow background supported the hypothesis that colour matching functions to deceive prey.     

Evolutionary changes in the integument of the onychophoran Plicatoperipatus jamaicensis (Peripatidae)

The dorsal integument of nearly all species of Peripatidae—one of the two major subgroups of Onychophora (velvet worms)—typically exhibits 12 plicae (=annuli) per segment. The only exception might occur in Plicatoperipatus jamaicensis, from which 24 putative plicae per segment have been reported. Hence, the number of plicae might have been duplicated in this species. If so, one would expect that the structure of the duplicated plicae would resemble that of all other onychophoran species, and that the structures commonly associated with the plicae, including crater‐shaped papillae and hyaline organs, would also have been duplicated. To clarify whether there was indeed such duplication, we compared the structure of the integument in embryos and adults of Pl. jamaicensis (with the putative number of 24 plicae per segment) and Principapillatus hitoyensis (with the common number of 12 plicae per segment). Our scanning electron microscopic data revealed that embryos of both species have 12 plicae per segment. While this number persists in adults of Pr. hitoyensis, 12 additional rows of papillae (=pseudoplicae) occur in the dorsal integument in adults of Pl. jamaicensis. These pseudoplicae differ from the typical plicae of other onychophorans in that they are not equipped with primary papillae and are situated in furrows between the true plicae, as evidenced by the position of hyaline organs and crater‐shaped papillae. Our data further show that the number of the ventrolateral plicae, crater‐shaped papillae, and hyaline organs is similar in the two species studied. This suggests that the plicae have not been duplicated in the integument of Pl. jamaicensis, but rather that additional pseudoplicae have been inserted between the 12 original plicae. These pseudoplicae might have led to a denser package of dermal papillae in the dorsal integument of Pl. jamaicensis, but the functional significance of this evolutionary change is unknown.