A while back in the Annals, I introduced the mysterious (but not mythical) third eye, made even more peculiar by unexpected findings in the Anolis pineal gland (Moore & Menaker 2011). In a later post, I discussed non-visual photoreception—responses to light that do not require image formation—along with some recent evidence that such responses may be tuned to photic habitat in Anolis (Moore et al. 2012). Now I’m connecting the dots: non-visual photoreception in the Anolis pineal gland appears to be adapted to photic habitat (Moore & Menaker 2012).
A riddle: What has four legs, eagle eyes, and can change colors?
Anoles are extremely visual animals, with vision being the primary sensory mechanism through which they perceive their surroundings. Accordingly, their vision is excellent, at least during the daytime. (“Eagle eyes” might be a bit misleading. A more accurate phrase might be “bifoveate retinae conferring excellent visual acuity and depth perception”). The amount of daytime light available for vision depends largely on the vegetative structure in the microhabitat. Indeed, many Anolis species occupy a distinct “photic habitat” due to sun/shade preferences. Variation in photic habitat provides a treasure trove of testable hypotheses for the visual ecologist. Is anole vision adapted to particular light environments? Is dewlap color selected for detectability in a given light environment? And so on.
I totally dig visual ecology, but I’m using it as bait to draw your attention to a closely related (but under-studied) relationship between the light habitat and physiology/behavior. Anoles, like all other animals, use light in ways that do not require visual images at all. These so-called “non-visual” responses to light are used for things like the dilation and constriction of the pupils, the control of circadian rhythms, and seasonal responses to daylength. Non-visual photoreception is processed in the brain through different pathways than those involved in the formation of images, so these responses to light can occur even if the animal is visually blind.
Interesting stuff, but here’s where habitat enters the picture. Non-visual responses to light are irradiance-dependent, meaning that whether or not there is a response, and what the response entails, depends on how much light there is. Bright light, for example, is a wake-up signal to the sleeping lizard, whereas dim light (e.g., moonlight) is less effective in eliciting arousal. However, “bright” and “dim” are relative measures, thus one might expect that the sensitivity of non-visual photoreception would be “tuned” to the overall light levels in the microhabitat. After all, light that seems dim in an open, unshaded habitat might correspond to the brightest midday light available in closed canopy forest. A mismatch between non-visual photosensitivity and habitat irradiance would impair non-visual photoreceptive “performance,” and could even lead to the misinterpretation of photic cues.
In a recent paper published in Journal of Comparative Physiology A, we showed that a non-visual behavioral response to light (the photic induction of locomotor activity) is correlated with habitat irradiance using four species of Puerto Rican anoles (A. cristatellus, A. gundlachi, A. pulchellus, A. krugi). Most diurnal animals respond to light by increasing their activity level. The best way to demonstrate this is to give light when the animal is inactive, i.e., at night. We developed a special device to continuously detect and record anole locomotor activity (walking, running, jumping, etc.) for weeks on end.
We quantified baseline activity levels during the day and night, then measured the increase in activity in response to light given at night. Species occupying relatively more shaded habitats were more sensitive to the effects of light (light induced more locomotor activity) as compared to closely related, ecomorphologically identical species occupying more brightly illuminated habitats. The differences were most pronounced at irradiance levels similar to natural twilight levels. This jives well with the notion that dawn is nature’s alarm clock, and that photosensitivity should be tuned to take advantage of morning light, whatever irradiance that may be in a given environment.
Still, there are a few gaps that need to be filled in to complete the story. (You’ll have to read the paper to find out what they are). Non-visual photoecology is still in its infancy, and the main challenge is to develop approaches to explore the links between the environment, non-visual photoreception, and fitness. If anyone’s interested in pursuing variations on this theme, I know a good post-doc for hire.
Yes, it’s true. A “third eye” does exist, not only in the ancient Hindu literature and the new age imagination, but in birds, amphibians, reptiles, fish, lampreys, and hagfishes. We’re talking about the pineal gland, a small organ located on top of the brain, just underneath the surface of the skull. Although it doesn’t have visual capabilities in the image-forming sense, it is intrinsically photosensitive, responding to light signals without any help from the lateral eyes. (Mammals, including humans, have a pineal gland too…but it has lost the ability to detect light).
Anoles, and some other lizards, actually have two “third eyes,” one being the pineal gland, and the other being the parietal eye, which can be seen in the picture above. Continue reading Surprises from the Anolis “Third Eye”