Light Perception in Two Strictly Subterranean Rodents: Life in the Dark or Blue?

BACKGROUND: The African mole-rats (Bathyergidae, Rodentia) are strictly subterranean, congenitally microphthalmic rodents that are hardly ever exposed to environmental light. Because of the lack of an overt behavioural reaction to light, they have long been considered to be blind. However, recent anatomical studies have suggested retention of basic visual capabilities. In this study, we employed behavioural tests to find out if two mole-rat species are able to discriminate between light and dark, if they are able to discriminate colours and, finally, if the presence of light in burrows provokes plugging behaviour, which is assumed to have a primarily anti-predatory function. METHODOLOGY/PRINCIPAL FINDING: We used a binary choice test to show that the silvery mole-rat Heliophobius argenteocinereus and the giant mole-rat Fukomys mechowii exhibit a clear photoavoidance response to full-spectrum ("white"), blue and green-yellow light, but no significant reaction to ultraviolet or red light during nest building. The mole-rats thus retain dark/light discrimination capabilities and a capacity to perceive short to medium-wavelength light in the photopic range of intensities. These findings further suggest that the mole-rat S opsin has its absorption maximum in the violet/blue part of the spectrum. The assay did not yield conclusive evidence regarding colour discrimination. To test the putative role of vision in bathyergid anti-predatory behaviour, we examined the reaction of mole-rats to the incidence of light in an artificial burrow system. The presence of light in the burrow effectively induced plugging of the illuminated tunnel. CONCLUSION/SIGNIFICANCE: Our findings suggest that the photopic vision is conserved and that low acuity residual vision plays an important role in predator avoidance and tunnel maintenance in the African mole-rats

Light perception in two mole-rat species, the silvery mole-rat \kur{(Heliophobius argenteocinereus)} and the giant mole-rat \kur{(Fukomys mechowii)}.

Sight in subterranean mammals living in a dark ecotope has generally been assumed as not needed and therefore greatly diminished in its function. Recent neuroanatomical studies demonstrate unexpected preservation of the visual system of several African mole-rats (Bathyergidae, Rodentia). Only a few behavioural studies, testing visual abilities and discussing their adaptive significance in these rodents, have been published to date. A spontaneous preference to light stimuli of two mole-rat species, the silvery mole-rat (Heliophobius argenteocinereus) and the giant mole-rat (Fukomys mechowii), was tested in this study. Assessed results showed convincingly that both species are able to perceive light. The following experiments provided the first behavioural support to the perception of short-wavelengths in this intensively studied group of subterranean rodents

Visual capabilities in subterranean rodents

This Ph.D. thesis focuses on the visual capabilities of subterranean African mole-rats (family Bathyegidae) and a potential role of their residual vision. We described basic visual capability of light/dark discrimination and capacity to perceive short to medium-wavelength light in the photopic range of intensities. Our behavioural findings revealed severe visual deficits, implying visually guided spatial orientation in molerats improbable. Our field study demostrated no light-correlated daily activitivy pattern of mole-rats in the natural habitat. We described very effective propagation of long wavelength light in breached burrows that can be detected by mole-rats for long distances, in contary to short wavelengths with very low propagation. Thus, an unique primary blue light perception, described only in African mole-rats among all mammalian species so far, has most probably no adaptive value and might be only a result of arrested cone development. Mole-rats effectively localized and plugged with soil illuminated sites under laboratory conditions, supporting the hypothesis that low acuity residual vision play an indispensable role in bathyergid anti-predatory behaviour and tunnel maintanance but not in spatial orientation

Light avoidance in the giant mole-rat <i>Fukomys mechowii</i> (a) and the silvery mole-rat <i>Heliophobius argenteocinereus</i> (b).

<p>Black bars represent the percentage of choices towards the dark and coloured bars towards the illuminated arm. The absolute number of choices made (dark: illuminated) and the statistical significance level of the response to the corresponding light are shown above each bar (***, P<0.001; **, P<0.01; *,P<0.05; NS, non significant).</p

Burrow plugging behaviour.

<p>Black and white bars represent the percentage of trials in which experimental animals did and did not plug the illuminated burrow, respectively. The absolute number of trials and the statistical significance level of the response are shown above each bar (***, P<0.001).</p

Spectra of the full-spectrum and monochromatic lights used in the experiments.

<p>The black line indicates the spectrum of the full-spectrum light produced by fluorescent tubes; coloured lines indicate the spectra of the monochromatic lights (note that the colour-code is symbolic, i.e., the colours do not exactly match to the spectra). The peak wavelengths are given for monochromatic lights. For clarity, all spectra are standardised by taking the maximum value within the measured wavelength interval as 10.</p

The experimental paradigms used in this study.

<p>(a–c) Different layouts of a binary-choice apparatus for testing nest building preference. (d) Diagram of an artificial burrow system used to evaluate burrow plugging behavior; the bulb icon marks the illuminated tunnel. A detailed description of the mazes and experimental protocols are given in the text.</p