Social costs enforce honesty of a dynamic signal of motivation

Understanding the processes that promote signal reliability may provide important insights into the evolution of diverse signalling strategies among species. The signals that animals use to communicate must comprise mechanisms that prohibit or punish dishonesty, and social costs of dishonesty have been demonstrated for several fixed morphological signals (e.g. colour badges of birds and wasps). The costs maintaining the honesty of dynamic signals, which are more flexible and potentially cheatable, are unknown. Using an experimental manipulation of the dynamic visual signals used by male veiled chameleons ( Chamaeleo calyptratus ) during aggressive interactions, we tested the idea that the honesty of rapid colour change signals is maintained by social costs. Our results reveal that social costs are an important mechanism maintaining the honesty of these dynamic colour signals—‘dishonest’ chameleons whose experimentally manipulated coloration was incongruent with their contest behaviour received more physical aggression than ‘honest’ individuals. This is the first demonstration, to the best our knowledge, that the honesty of a dynamic signal of motivation—physiological colour change—can be maintained by the social costliness of dishonesty. Behavioural responses of signal receivers, irrespective of any specific detection mechanisms, therefore prevent chameleon cheaters from prospering.

Background colour matching in a wild population of Alytes obstetricans

The capacity for physiological colour change has long been described in anuran amphibians. Camouflage against predators seems to be the most relevant function of dynamic changes in skin colour of frogs, but key aspects such as the rate at which these changes occur, or the specific colour components involved are not completely clear. Whereas most research on the topic has been reported on tree frogs in laboratory conditions, studies in other anurans or in the field are much scarcer. Here we show a potentially plastic, adaptive response in coloration of common midwife toads, Alytes obstetricans, from a population of central Portugal, whose pigmentation varied with their natural backgrounds. Using quantitative image analysis, we compared hue, saturation and brightness of dorsal skin coloration of toads and the colour of the area of ground immediately around them. We found a positive correlation between coloration of toads and background colour for the three components of the colour. As well as other anuran species, A. obstetricans might adjust skin coloration to match the surrounding environment, thus benefitting from short-term reversible crypsis strategies against predators. A less supported hypothesis would be that toads accurately select matching backgrounds to improve concealment as an antipredatory strategy.

The lantern shark's light switch: turning shallow water crypsis into midwater camouflage

Bioluminescence is a common feature in the permanent darkness of the deep-sea. In fishes, light is emitted by organs containing either photogenic cells (intrinsic photophores), which are under direct nervous control, or symbiotic luminous bacteria (symbiotic photophores), whose light is controlled by secondary means such as mechanical occlusion or physiological suppression. The intrinsic photophores of the lantern shark Etmopterus spinax were recently shown as an exception to this rule since they appear to be under hormonal control. Here, we show that hormones operate what amounts to a unique light switch, by acting on a chromatophore iris, which regulates light emission by pigment translocation. This result strongly suggests that this shark's luminescence control originates from the mechanism for physiological colour change found in shallow water sharks that also involves hormonally controlled chromatophores: the lantern shark would have turned the initial shallow water crypsis mechanism into a midwater luminous camouflage, more efficient in the deep-sea environment.

Flexibility in the colouration of the meninx (brain covering) in the guppy (Poecilia reticulata): investigations of potential function

Many organisms can change the apparent colour of their bodies by altering the aggregation of pigment in chromatophores in a process known as physiological colour change. In this study, we investigate a previously unstudied example of physiological colour change, from clear to black, of a brain covering, or meninx, in the guppy ( Poecilia reticulata Peters, 1859). UV protection in bright light was our primary hypothesis for the function of the meningeal colour, with a cost of increased conspicuousness to avian predators selecting for plasticity in the trait. An alternate hypothesis was that this flexible trait could be a physiological by-product of stress. Thus, we investigated the response of meningeal colour to light, stress, and simulated predator attacks, and also whether the black meninx affected conspicuousness to potential predators. Meningeal response to higher light levels did not differ from baseline responses. However, we did find that stress induced a sex-biased, rapid darkening of the meninx; this darkening then declined over time. These results suggest that meningeal blackness could be used as a novel, noninvasive indicator of stress level in guppies. We found no evidence for a role of predation in meningeal colour: meninx colour did not respond to the presence of a predator model and human “predators” detected similar numbers of guppies with black meninges and guppies with clear meninges.

Camouflage, communication and thermoregulation: lessons from colour changing organisms

Organisms capable of rapid physiological colour change have become model taxa in the study of camouflage because they are able to respond dynamically to the changes in their visual environment. Here, we briefly review the ways in which studies of colour changing organisms have contributed to our understanding of camouflage and highlight some unique opportunities they present. First, from a proximate perspective, comparison of visual cues triggering camouflage responses and the visual perception mechanisms involved can provide insight into general visual processing rules. Second, colour changing animals can potentially tailor their camouflage response not only to different backgrounds but also to multiple predators with different visual capabilities. We present new data showing that such facultative crypsis may be widespread in at least one group, the dwarf chameleons. From an ultimate perspective, we argue that colour changing organisms are ideally suited to experimental and comparative studies of evolutionary interactions between the three primary functions of animal colour patterns: camouflage; communication; and thermoregulation.

Female dimorphism and physiological colour change in the damselfly Argia vivida Hagen (Odonata: Coenagrionidae)

Female Argia vivida appear as two distinct colour morphs in each of two populations studied in British Columbia, Canada. Males and both female morphs also experience a temperature-related physiological colour change. Individuals are "dark phase" at ambient shade temperatures below approximately 20 °C and change to "bright phase" at temperatures above 20 – 24 °C, particularly when basking. Individuals of either colour phase will attempt to mate. Bright phase males reflect not only visible light but also ultraviolet light. Observations of marked individuals and experiments in which males were offered live females (singly or as a pair containing each morph) pinned to long grass stems indicated that males do not show a preference for either female colour morph. The two female morphs do not differ in size, nor do males that mate with each morph. A male removal experiment revealed no change in the relative number of females of each morph that mated each day, suggesting that the morphs do not differ in their ability to attract males or to avoid excessive matings. Several social, ecological, and genetic explanations for sustaining the female dimorphism in the population are discussed.

Evidence for the participation of a melanin-concentrating hormone in physiological colour change in the eel

ABSTRACT The hormonal and nervous control of colour change in the eel has been investigated. The only bioactive forms of MSH found in eel pituitary extracts or secreted by eel pituitary cultures were forms of α-MSH; no β-MSH was detected. After transfer of eels from a black to a white background, the melanin concentration in skin melanophores was accompanied by a rapid decline in plasma α-MSH titres. Hypophysectomy resulted in melanin concentration, and pituitary extracts injected into hypophysectomized eels caused melanin dispersion. This effect was eliminated if the pituitary extracts were first incubated with a specific α-MSH antiserum or if the antiserum was injected into the hypophysectomized eel. However, injection of α-MSH antiserum into intact, black-adapted eels failed to result in melanin concentration although the same antiserum was effective in causing pallor in black-adapted toads. Partially purified preparations of teleost melanin-concentrating hormone (MCH), free from catecholamines, induced melanin concentration when injected into black-adapted eels and this effect was significantly potentiated by injections of α-MSH antiserum. The denervation of melanophores on the pectoral fin had only a slight effect on the responses of the melanophores to humoral agents. It is concluded that the control of physiological colour change in the eel is largely hormonal, and involves the antagonistic effects of α-MSH and a melanin-concentrating agent which is probably MCH. J. Endocr. (1984) 102, 237–243