When Glen Jeffery first took possession of a huge bag full of reindeer eyes, he didn’t really want them.

Jeffery is a neuroscientist from University College London who studies animal vision, and his Norwegian colleagues had been urging him to study the eyes of reindeer. They wanted to know how these animals cope with three months of constant summer sunlight and three months of perpetual winter darkness. “I thought it was a dumb idea,” says Jeffery. The animals would probably adapt to the changing light through some neurological trick. The eyes weren’t the right place to look.

But the Norwegians persisted, and they eventually sent him a bag full of eyes, taken from animals killed by local Sami herders. The eyes were divided into two sets—one from animals killed in the summer, and another from those killed in the winter. Jeffery started dissecting them. “I opened them up and went: Jesus Christ!” says Jeffery. “Hang on. They’re a different colour”

In the summer, reindeer eyes are golden. In the winter, they become a deep, rich blue. “That was completely unexpected,” says Jeffery.

That was 13 years ago. Since then, he has been working to understand the secrets behind the chameleon-like eyes, along with Karl-Arne Stokkan from the University of Tromsø and others.

The bit that actually changes colour is the tapetum lucidum or “cat’s eye”—a mirrored layer that sits behind the retina. It helps animals to see in dim conditions by reflecting any light that passes through the retina back onto it, allowing its light-detecting cells a second chance to intercept the stray photons. The tapetum is the reason why mammal eyes often glow yellow if you photograph them at night—you’re seeing the camera’s flash reflecting back at you.

Most mammals have a golden tapetum, and so do the reindeer in summer. So why does this layer become blue in winter? Through years of dissections and measurements, Jeffrey’s team think that they have the answer. And it begins in darkness.

View Images Credit: Alexandre Buisse

In dark conditions, muscles in your irises contract to dilate your pupils and allow more light into your eyes. When it’s bright again, the irises widen and the pupils shrink. The same thing happens in reindeer, but the interminable Arctic winter forces their pupils dilate for months rather than hours. Over time, this constant effort blocks the small vessels that drain fluid out of the eyes. Pressure builds up inside the eyeballs, and they start to swell. “The animal’s moving towards glaucoma,” says Jeffery.

These events also change the tapetum. This layer is mostly made up a collagen, a protein whose long fibres are arranged in orderly rows. As the pressure inside the eye builds up, the fluid between the collagen fibres gets squeezed out, and they become more tightly packed. The spacing of these fibres affects the type of light they reflect. With the usual gaps between them, they reflect yellow wavelengths. When squeezed together, they reflect… blue wavelengths.

So: as reindeer spend months of darkness, their permanently dilated pupils lead to swollen eyes, compressing the fibres in their tapetum and changing the colour of light they reflect.

The team also think that this makes the eyes more sensitive. They tested the retinas of reindeer eyes, both isolated ones and those still in the heads of live, anaesthetised animals, and found that the blue winter ones are at least a thousand times more sensitive to light than the golden summer ones.

Jeffery explains that when yellow light reflects off the tapetum, most of it bounces straight out again. The retina gets just one more chance to intercept it. But blue light gets scattered. “Instead of the photons bouncing back out of the eye, they bounce around and gets captured, which increases the sensitivity” says Jeffery.

But other scientists aren’t convinced by this explanation. Dan-Eric Nilsson, a vision expert from Lund University, is excited that the sensitivity of the reindeer eyes and the colour of their tapetum change with the seasons. Both are interesting, but the latter does not explain the former.

Here’s his argument: Let’s say that the retina captures around 50 percent of the light that enters the eye, and that the tapetum reflects all of the rest. The retina captures half of these reflections, ending up with 75 percent of the original total. Even if you assume that the retina was infinitely inefficient, the most the tapetum could do is to double its sensitivity. And Jeffery’s team found that the retina becomes around a thousand times more sensitive in winter. “They’ve found an interesting phenomenon, but failed in explaining it,” says Nilsson. He suspects that, instead, the reindeer is changing the levels of light-sensitive pigments in its retina.

Trevor Lamb, another eye expert at the Australian National University, agrees. “I wouldn’t be at all surprised if the retina managed to increase its sensitivity during winter through some kind of intra-retinal changes, quite separate from the tapetal ones,” he says, “but that is pure speculation on my part.”

But Jeffery’s team has another piece of evidence for their hypothesis—one which they mention briefly in their new paper but will outline more fully in a future one. “We got halfway through this project and everything’s cruising brilliantly, and we suddenly hit a brick wall,” he says. “We suddenly found animals with a green tapetum.”

It turned out that these reindeer had been bought from Sami herders and kept in large pens, where they could just about see the sodium street-lights of nearby towns. Their pupils partly dilated during the winter, the pressure in their eyes increased a little, their collagen fibres became slightly squeezed together, and their tapetums stopped halfway along their yellow-to-blue transformation. Et voila. Green tapetum.

“And we measured the sensitivity in their eyes,” says Jeffery. “Way down.”

It could still be that the changes in the eyes are independently changing the colour of the tapetum and the sensitivity of the retina. It’ll require more evidence to link the two, but both observations alone are still pretty cool. As Nilsson say, “I am not aware of any other seasonal changes in the visual optics. In that respect, this is a novel and exciting discovery.”

Reference: Stokkan, Folkow, Dukes, Nevue, Hogg, Siefken, Dakin & Jeffery. 2013. Shifting mirrors: adaptive changes in retinal reflections to winter darkness in Arctic reindeer. Proc Roy Soc B http://dx.doi.org/10.1098/rspb.2013.2451

PS: If, like me, you do a Google image search for tapetum lucidum pictures, you’ll find several images where the eyes look topaz, rather than yellow. This is very different from the deep, rich blue of the reindeer’s winter eyes. Partly, it happens because digital cameras automatically adjust the pictures they take. But it’s also because golden tapetums do have a topaz fringe, which takes over the reflections if you photograph the animal from an angle.