The spectral transmission of ocular media suggests ultraviolet sensitivity is widespread among mammals

Abstract

Although ultraviolet (UV) sensitivity is widespread among animals it is considered rare in mammals, being restricted to the few species that have a visual pigment maximally sensitive (λmax) below 400 nm. However, even animals without such a pigment will be UV-sensitive if they have ocular media that transmit these wavelengths, as all visual pigments absorb significant amounts of UV if the energy level is sufficient. Although it is known that lenses of diurnal sciurid rodents, tree shrews and primates prevent UV from reaching the retina, the degree of UV transmission by ocular media of most other mammals without a visual pigment with λmax in the UV is unknown. We examined lenses of 38 mammalian species from 25 families in nine orders and observed large diversity in the degree of short-wavelength transmission. All species whose lenses removed short wavelengths had retinae specialized for high spatial resolution and relatively high cone numbers, suggesting that UV removal is primarily linked to increased acuity. Other mammals, however, such as hedgehogs, dogs, cats, ferrets and okapis had lenses transmitting significant amounts of UVA (315-400 nm), suggesting that they will be UV-sensitive even without a specific UV visual pigment.

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Research
Cite this article: Douglas RH, Jeffery G. 2014
The spectral transmission of ocular media
suggests ultraviolet sensitivity is widespread
among mammals. Proc. R. Soc. B 281:
20132995.
http://dx.doi.org/10.1098/rspb.2013.2995
Received: 15 November 2013
Accepted: 21 January 2014
Subject Areas:
neuroscience
Keywords:
vision, lens, transmission, mammal, ultraviolet
sensitivity, retina
Author for correspondence:
R. H. Douglas
e-mail: r.h.douglas@city.ac.uk
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rspb.2013.2995 or
via http://rspb.royalsocietypublishing.org.
The spectral transmission of ocular media
suggests ultraviolet sensitivity is
widespread among mammals
R. H. Douglas1and G. Jeffery2
1
Department of Optometry and Visual Science, City University London, Northampton Square,
London EC1V 0HB, UK
2
Institute of Ophthalmology, University College London, 11-43 Bath Street, London EC1V 9EL, UK
Although ultraviolet (UV) sensitivity is widespread among animals it is con-
sidered rare in mammals, being restricted to the few species that have a
visual pigment maximally sensitive (
l
max
) below 400 nm. However, even ani-
mals without such a pigment will be UV-sensitive if they have ocular media
that transmit these wavelengths, as all visual pigments absorb significant
amounts of UV if the energy level is sufficient. Although it is known that
lenses of diurnal sciurid rodents, tree shrews and primates prevent UV from
reaching the retina, the degree of UV transmission by ocular media of most
other mammals without a visual pigment with
l
max
in the UV is unknown.
We examined lenses of 38 mammalian species from 25 families in nine
orders and observed large diversity in the degree of short-wavelength trans-
mission. All species whose lenses removed short wavelengths had retinae
specialized for high spatial resolution and relatively high cone numbers,
suggesting that UV removal is primarily linked to increased acuity. Other
mammals, however, such as hedgehogs, dogs, cats, ferrets and okapis had
lenses transmitting significant amounts of UVA (315 –400 nm), suggesting
that they will be UV-sensitive even without a specific UV visual pigment.
1. Introduction
The range of wavelengths an animal perceives depends on the spectrum available
in the environment, the degree to which this is transmitted though the ocular
media and the visual pigments within the retina. The spectrum that humans
see during the day, using three cone visual pigments absorbing maximally
(
l
max
) at 420, 534 and 563 nm [1], spans approximately 400– 700 nm. Adult
humans are insensitive to shorter, ultraviolet (UV) wavelengths as these are
absorbed by the lens [2–5] and hence never reach the retina.
The range of wavelengths visible to other animals is often very different
from that of man due largely to their possession of visual pigments absorbing
elsewhere in the spectrum. Many species, for example, possess visual pigments
with
l
max
below 400 nm, and the resultant UV-sensitivity is relatively wide-
spread among invertebrates [6– 8], birds, fish, reptiles and amphibians [9,10].
Among mammals, such UV-sensitive visual pigments are relatively rare and
have only been described in some rodents [11– 18], a mole [19], several marsu-
pials [20–23] and some bats [24–27]. Such animals have lenses that, unlike
those of humans, transmit short wavelengths well. UV sensitivity in mammals,
in comparison to other animals, is thus thought to be the exception.
Although visual pigments are usually characterized by their
l
max
, the wave-
length range absorbed by them is in fact broad and displays a secondary
absorption maximum in the UV (the cis-peak or b-band). Thus, all photo-
receptors can potentially absorb significant amounts of UV and any animal
with ocular media that are transparent to UV light will inevitably be sensitive
to these wavelengths even if they do not possess a visual pigment with
l
max
in
this part of the spectrum [9] (figure 1).
&2014 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution
License http://creativecommons.org/licenses/by/3.0/, which permits unrestricted use, provided the original
author and source are credited.

Therefore, if the UV-absorbing lens of humans is removed
following cataract surgery or traumatic injury, and not replaced
by a UV-absorbing prosthetic, they report vivid and detailed
vision in the UV [6,31–33]. Similarly, despite the absence of a
visual pigment with
l
max
in the UV, the reindeer retina responds
electrophysiologically below 400 nm [34] and circadian rhythms
in the Syrian hamster can be entrained by wavelengths below
400 nm[35– 40], simply because they both have lenses that trans-
mit significant amount of light below 400 nm ratherthan a visual
pigment with
l
max
in the UV. Likewise, a phyllostomid flower
bat with a UV-transparent lens is able to respond behaviourally
to UV even in scotopic conditions using the b-band of its rod
pigment [41]. A degree of UV sensitivity in the absence of a
photoreceptor absorbing maximally in this part of the spectrum
is therefore not infrequent.
The spectral transmission of the ocular media (cornea, lens,
aqueous and vitreous humour) at short wavelengths is deter-
mined by their structural components, thickness and any
specific short-wave absorbing pigments they contain [42]. No
structure will transmit significant amounts of light below
about 300 nm owing to absorption by its nucleic acids and
structural protein components, for example aromatic amino
acids. With the exception of some fish corneas that absorb
blue/green light [43–45], most corneas are thin and unpig-
mented, transmitting UV radiation down to around 300 nm.
Aqueous and vitreous humours are similarly transparent.
Lens transmission, however, is very variable. In some species,
the lens lets through almost as much UV as the cornea, while
in others it can remove all UV and some of the blue, appearing
visibly yellow. Thus, although oil droplets in birds, for example,
prevent short wavelengths from reaching the outer segments of
some cones, and pigments such asthehuman macular pigment
absorb bluelight, the lens is the filter that determines the cut-off
in the UV in almost all species (see the electronic supplementary
material, S1).
Unfortunately,detailed information about the spectral trans-
mission ofmost mammalian lenses is lacking. The only ones that
have been examined are those that seem obviously interesting.
At one extreme, the lenses of diurnal primates [5,46–49], tree
shrews [50,51] and sciurid rodents [12,39,52– 58] are various
shades of yellow, removing all radiation below 420–470 nm.
At the other extreme, species with visual pigments with
l
max
in the UV have lenses maximally transparent to UV radiation,
transmitting most light down to 320 –340 nm [3,4,12,16,18,
19,23,25,36,37,59 –64]. However, little is known about the wave-
lengths transmitted by the lenses of mammals between these
two extremes. Although the lenses of some have been reported
as containing no short-wavelength-absorbing pigment [54],
reliable quantitative transmission data from intact lenses are
only available only for the Syrian hamster (Mesocricetus auratus)
[35–39], pig (Sus scrofa) [4], rabbit (Oryctolagus cuniculus)
[3,65–68] and reindeer (Rangifer tarandus)[34].
Here, we examine the spectral transmission of the lenses of
38 mammalian species belonging to 25 families in nine orders,
most never examined before, and show a variety of degrees
of shortwave transmission. Perhaps surprisingly, many let
through significant amounts of shortwave radiation, suggesting
that a degree of UV sensitivity is widespread among mammals.
2. Material and methods
Animals were obtained from various sources such as abattoirs,
zoos, veterinary practices and scientific establishments (see
Acknowledgements). They had either been used for other scien-
tific procedures, sacrificed for food production, died naturally or
were put down owing to injury or illness. No animals were killed
specifically for this project. Eyes were obtained either immedi-
ately following death, or soon thereafter, and were either used
immediately or frozen dry for several days before thawing. Vari-
able numbers of lenses were available for each species and in
four species a range of lens sizes/ages were examined (see
table 1 for details).
Lenses, and usually corneas, were removed from the eye,
briefly rinsed in phosphate-buffered saline (PBS) and mounted
in purpose-built holders in air in front of an integrating sphere
within a Shimadzu 2101 UVPC spectrophotometer. Vitreous
humour was also removed from the eyes of some animals with
a syringe and placed in a standard quartz cuvette within the
same apparatus. Transmission at 700 nm was set to 100% and
ocular media scanned at 1 nm intervals from 300 to 700 nm.
To determine the effect of freezing on lens transmission, three
fresh bovine lenses were scanned soon after death, frozen in air at
2258C for 4 days, thawed and rescanned.
The pigments responsible for lens pigmentation were also
extracted and spectrally characterized for six species (see the
electronic supplementary material, S4).
3. Results
Although the cornea and vitreous humour were not exam-
ined in all species, when they were, in line with previous
observations [42], the lens always removed more short-
wavelength radiation than either the cornea or the vitreous
(see the electronic supplementary material, S1).
Freezing had no significant effect on lens transmission,
allowing data from both fresh and previously frozen lenses
to be compared (figure 2).
The spectral transmission of the lenses of some of the
species studied here had been examined previously; pig [4],
tree shrew (Tupaia glis) [50], rabbit [3,65 –68], mouse (Mus mus-
culus) [3,4,63,64], brown rat (Rattus norvegicus) [3,4,12,36,37,60],
grey squirrel (Sciurus carolinensis) [54,58], prairie dog (Cynomys
ludovicianus) [55–56], flying squirrel (Glaucomys volans) [56],
marmoset (Callithrix jacchus)[49],squirrelmonkey(Saimiri
0
20
40
60
80
100
0
0.2
0.4
0.6
0.8
1.0
300 400 500 600 700
% transmission
normalized absorbance
wavelength (nm)
Figure 1. The absorption spectra of the visual pigments of the ferret and the
spectral transmission of its lens. The absorption maxima of the visual
pigments (rods—505 nm; cones—430 and 558 nm) are taken from
Calderone & Jacobs [28] and the visual pigments templates of Govardovskii
et al. [29] (solid lines) have been fitted to them using the methods described
in Hart et al. [30]. The lens transmission (dotted line) is taken from this
study. As all the visual pigments absorb significant amounts of UV radiation
and the lens transmits in this part of the spectrum, the ferret is likely to
perceive such short wavelengths.
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2

Table 1. Summary of mammalian lenses examined ranked by the amount of UVA they transmit. ‘50%T’ is the wavelength at which the lens transmits 50% of
the incident illumination. ‘%UVA transmitted’ is a measure of the proportion of light between 315 and 400 nm that is transmitted by the lens (see the
electronic supplementary material, S2). For most species, lens transmission and axial diameter ( pathlength) varied little between individuals and averages are
shown. Where there were significant differences between individuals, ranges are given. Where the transmission of the lens varied with lens size/age, the % UVA
on the retina was calculated using specific ages/lens sizes as described in footnotes.
order family species
number of
lenses
pathlength
(mm)
50%T
(nm)
%UVA
transmitted
Rodentia Muridae mouse (Mus musculus) 29 1.9–2.8 313–337 81.4
a
Rodentia Muridae black rat (Rattus rattus) 11 3.7–5.2 317–372 80.5
b
Erinaceomorpha Erinaceidae hedgehog (Erinaceus
europaeus)
4 3.0 326 65.5
Carnivora Canidae dog (Canis lupus familiaris)
(labrador)
2 5.0 335 61.3
Chiroptera Pteropodidae Livingstone’s fruit bat
(Pteropus livingstonii)
4 5.0–6.0 332–422 60.8
c
Carnivora Felidae cat (Felis catus) 6 7.0 345 58.9
Carnivora Mustelidae ferret (Mustela putorius furo) 4 3.9 344 56.1
Rodentia Muridae brown rat (Rattus norvegicus) 2 4.2 339 55.8
Artiodactyla Giraffidae okapi (Okapia johnstoni) 2 7.0 355 53.4
Artiodactyla Suidae pig (Sus scrofa) 5 5.5 375 43.6
Rodentia Caviidae guinea pig (Cavia porcellus) 11 3.7 377 34.6
Carnivora Ailuridae red panda (Ailurus fulgens) 1 5.8 386 30.2
Rodentia Sciuridae flying squirrel
(Glaucomys volans)
2 4.9 423 29.3
Chiroptera Pteropodidae Rodrigues flying fox
(Pteropus rodricensis)
1 4.8 388 28.1
Artiodactyla Cervidae reindeer (Rangifer tarandus) 5 10.1 384 26.5
Artiodactyla Cervidae pudu
´(Pudu puda) 2 7.0 386 25.0
Artiodactyla Bovidae cattle (Bos primigenius) 8 11.1 384 22.1
Artiodactyla Bovidae sheep (Ovis aries) 4 7.7 393 15.2
Rodentia Dasyproctidae agouti (Dasyprocta punctata) 1 6.1 406 15.0
Lagomorpha Leporidae rabbit (Oryctolagus cuniculus) 2 6.7 392 12.7
Artiodactyla Tragulidae java mouse deer
(Tragulus javanicus)
2 9.0 403 12.4
Artiodactyla Bovidae Arabian oryx (Oryx leucoryx) 1 10.3 400 8.5
Artiodactyla Camelidae alpaca (Vicugna pacos) 5 10.2 405 6.0
Perissodactyla Equidae horse (Equus ferus caballus) 1 12.0 416 4.6
Primates Cebidae squirrel monkey
(Saimiri sciureus sciureus)
2 4.6 420 2.8
Primates Lemuridae ring-tailed le
´mur
(Lemur catta)
1 6.5 425 2.0
Carnivora Herpestidae meerkat (Suricata suricatta) 3 2.4–3.4 420–436 1.7
d
Primates Callitrichidae marmoset (Callithrix jacchus) 1 3.0 427 0.9
Artiodactyla Bovidae lowland anoa
(Bubalus depressicornis)
1 8.0 478 0.6
Rodentia Sciuridae ground squirrel
(Urocitellus richardsonii)
2 3.1 462 0.6
Primates Cercopithecidae macaque (Macaca fascicularis) 5 3.3 424 0.5
(Continued.)
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3

sciureus sciureus)[46]andmacaque(Macaca fascicularis)[48].Our
data for these species agreed with the previously published spec-
tra. They are presented here to validate our method, facilitate
direct comparison with novel data and allow further analysis.
The spectral transmission of representative lenses is shown in
figure 3 and equivalent scans for all species are shown in the elec-
tronic supplementary material, S3. The spectral properties of the
mammalian lenses examined ranged from those in young murid
rodentsaswellasjuvenilehedgehogs,whichtransmittedlarge
amounts of UV radiation (50% transmission 310– 320 nm), to
those of primates, sciurid rodents, meerkats and tree shrews
that were visibly yellow and prevented UV radiation from reach-
ing the retina (50% transmission 424–465 nm). All other
mammals had lenses whose spectral transmission lay between
these two extremes (table 1 and figure 3; also see the electronic
supplementary material, figure S3a–d).
The degree of UV radiation transmitted by the lens is
traditionally expressed as the wavelength of 50% transmission.
However, this measure can be misleading as the short-wave-
length cut-off is sometimes steep, but at other times gentle.
Thus, although the flying squirrel and the macaque both have
a similar wavelength of 50% transmission (423 –424 nm), their
spectral characteristics at short wavelengths are in fact quite
different (see the electronic supplementary material, figure 3c).
A better indication of the potential for UV vision is given by
the proportion of UVA (315 –400 nm) that is transmitted by the
lens (table 1; see the electronic supplementary material, S2).
Forfourspecies(Pteropus livingstonii,Rattus rattus,Mus mus-
culus and Suricata suricatta), lenses from a range of ages/sizes
were available and exhibited decreased short-wavelength trans-
mission in older/larger lenses. Data are shown only for the rat
andmouse(figure4)asthelargestnumberofdifferentlysized
lenses were available for them. Similar trends were shown by
lesser numbers of Livingston’s bats (n¼4) and meerkats (n¼3).
The eyes of the Alaotran gentle lemur and the ring-tailed
lemur, apart from containing a distinctly yellow coloured
Table 1. (Continued.)
order family species
number of
lenses
pathlength
(mm)
50%T
(nm)
%UVA
transmitted
Primates Atelidae red-faced spider monkey
(Ateles paniscus)
1 3.8 438 0.4
Primates Callitrichidae golden lion tamarin
(Leontopithecus rosalia)
1 3.0 441 0.4
Scandentia Tupaiidae Tree shrew (Tupaia glis) 1 3.2 435 0.3
Primates Lemuridae Alaotran gentle lemur
(Hapalemur alaotrensis)
1 5.9 425 0.3
Rodentia Sciuridae grey squirrel
(Sciurus carolinensis)
2 3.6 441 0
Rodentia Sciuridae prairie dog
(Cynomys ludovicianus)
7 3.6 463 0
Primates Cebidae capuchin (Cebus apella) 1 3.9 426 0
a
Aged 69 –72 days with lens pathlength 2.2 mm.
b
Pathlength 3.8 mm.
c
Pathlength 5.0 mm.
d
Pathlength 3.4 mm.
0
20
40
60
80
100
300 400 500 600 700
% transmission
wavelen
g
th (nm)
Figure 2. Average spectral transmission of three bovine lenses before (solid
line) and after (dashed line) four days of freezing.
0
20
40
60
80
100
300 350 400 450 500
% transmission
wavelen
g
th (nm)
Figure 3. Representative average spectral transmission curves at short wave-
lengths of the lenses from 10 mammalian species. Most curves are the
averages of all available lenses. However, for the black rat and meerkat indi-
viduals of a variety of lens sizes were scanned; the data shown for the two
species are for young and old animals, respectively. From left to right at 50%
transmission they are (n, lens axial diameter in millimetres); young black rats
(2, 3.8), cat (6, 7.0), okapi (2, 7.0), cattle (8, 11.1), rabbit (2, 6.7), Arabian
oryx (1, 10.3), squirrel monkey (2, 4.6), Alaotran gentle lemur (1, 5.9), adult
meerkat (1, 3.4) and prairie dog (7, 3.6). All scans were zeroed at 700 nm.
rspb.royalsocietypublishing.org Proc. R. Soc. B 281: 20132995
4

lens, on dissection revealed a bright yellow substance within
the eye. Strepsirrhine primates are known to have yellow ribo-
flavin-based tapeta [69], which is almost certainly the source of
this pigmentation.
A pigment absorbing maximally at 357– 369 nm was
extracted from the lenses of six species with yellow lenses
and identified as 3-hydroxykynurenine glucoside in two
(see the electronic supplementary material, S4).
4. Discussion
(a) Diversity of ultraviolet transmission by
mammalian lenses
As expected, the transmission of short wavelengths by the
mammalian lens varies considerably between species. At one
extreme, as has previously been reported, species with visual
pigments absorbing maximally in the UV– for example murid
rodents–transmit up to 80% of UVA radiation (figure 3 and
table 1; see also the electronic supplementary material, S3).
The most UV-transparent lens observed outside of such animals
belongs to the European Hedgehog (Erinaceus europeus;seethe
electronic supplementary material, figure S3b). Interestingly,
preliminary evidence suggests that the closely related Southern
white-breasted hedgehog (Erinaceus concolor) may in fact pos-
sess a visual pigment with
l
max
below 400 nm (M. Glo
¨smann
2013, personal communication). In stark contrast, the lenses of
mature diurnal primates, sciurid rodents, tree shrews and
meerkats contain a pigment absorbing maximally around
360– 370 nm (see the electronic supplementary material, S4).
Consequently, they absorb all UV radiation and a considerable
amount of blue light, appearing visibly yellow (figure 3 and
table 1; see also the electronic supplementary material, S3).
Although it is well established that sciurid rodents and diurnal
primates have yellow lenses, we have expanded the number of
species within these orders known to have such lenses, and
their presence in meerkats is a novel observation.
However, most mammals appear to have lenses between
these two extremes that transmit variable amounts of short-
wave radiation (figure 3 and table 1; see also the electronic
supplementary material, S3). Relatively large lenses like those
of the horse (Equus ferus caballus), alpaca, oryx, anoa (Bubalus
depressicornis) and mouse deer remove the vast majority of
the UV, although as they remove little visible radiation, they
do not appear obviously yellow. On the other hand, animals
such as the cat, dog, ferret and okapi have lenses that transmit
only slightly less UVA than those of some murid rodents
(figure 3 and table 1; see also the electronic supplementary
material, S3).
As expected, species that are at least partially nocturnal
generally have lenses transmitting UV, while those that
are mainly diurnal prevent such wavelengths reaching the
retina. For example, while diurnal sciurid rodents have
yellow lenses that remove all UV, the nocturnal flying squirrel
has a clear lens [56] that transmits significant amounts of
UVA (table 1; see also the electronic supplementary material,
figure S3c). However, such a demarcation is not absolute and
some animals, like the okapi, can be exposed to relatively
high amounts of daylight while having lenses that transmit
relatively large amounts of UV.
(b) Lens transmission indicates that a degree of
ultraviolet sensitivity may be widespread among
mammals
Only species with UV-transparent lenses and a visual pig-
ment with
l
max
below 400 nm are usually considered UV
sensitive. However, as all visual pigments have a degree of
photosensitivity at such short wavelengths, an animal with
a lens transmitting UV radiation will inevitably be sensitive
in this part of the spectrum, even in the absence of a specific
UV-absorbing visual pigment.
Species are ranked according to the amount of UVA trans-
mitted by the lens in table 1. A previous study has shown that
the reindeer, whose lens transmits 26.5% of UVA and which
does not have a visual pigment with
l
max
below 400 nm,
nevertheless responds electrophysiologically to 372 nm light
[34]. It therefore seems likely that species with similar or
0
20
40
60
80
100
(a)
(b)
(c)
300 400 500 600 700
% transmission
wavelength (nm)
310
320
330
340
350
360
370
380
3.5 4.0 4.5 5.0 5.5
50% transmission
pathlength (mm)
310
315
320
325
330
335
340
345
50% transmission
0 100 200 300 400 500 600
a
g
e (da
y
s)
Figure 4. Lens transmission asa function of lens size/age in rodents. (a) Spectral
transmission of 11 black rat (R. rattus) lenses ranging in axial length between
3.7 and 5.2 mm. (b) Wavelength of 50% transmission as a function of lens
size for all the lenses shown in (a). The data are fit by y¼43.992xþ
149.68 (R
2
¼0.9062). The dashed line is an approximation of the relationship
expected if pathlength were the only factor affecting transmission. (c)Average
wavelength of 50% lens transmission (+1 s.d.) of mice (M. musculus)of
known age; 40 (n¼3), 70 (n¼8), 265 (n¼4) and 564 (n¼6) days.
The data are fit by y¼0.0443xþ311.1 (R
2
¼0.9634).
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5

more UV lens transmission, such as cattle, pig, ferret, dog,
okapi and cat, for example, will also be sensitive at these
short wavelengths (table 1).
The realization that many mammals have some UV sensi-
tivity may be important for understanding aspects of their
behaviour as they could be responding to visual signals
undetectable to humans. It may also have implications for
the lighting conditions of captive and domestic species. On
the one hand, some UV may be required for normal behav-
iour, while on the other, excessive UV exposure might put
species with UV-transparent ocular media at increased risk
of retinal damage (see below).
(c) The nature of ultraviolet sensitivity without a
l
max
at short wavelengths
It might be argued that UV perception not mediated by a
visual pigment with
l
max
in this part of the spectrum is in
some way not ‘real’ UV sensitivity. However, nobody ques-
tions a human’s ability to see red light with a wavelength
of 700 nm, despite the fact that our long-wavelength sensitive
cone absorbs maximally at wavelengths more than 100 nm
removed from this.
Although all visual pigments can absorb UV radiation, the
way the signals generated by the photoreceptors to such wave-
lengths are processed is not known. Thus, animals without a
visual pigment with
l
max
in the UV will probably be unable
to distinguish UV as a separate colour. Aphakic humans, for
example, report UV as appearing like a desaturated (whitish)
blue-violet [6].
The extent of UV sensitivity in animals with UV-transparent
ocular media but without a specific UV visual pigment is also
uncertain. However, it is probable that such animals will be
less sensitive at these wavelengths than species that do have
such a visual pigment, although the photopic sensitivity of
aphakic humans [6] and reindeer [34] to UV light is surprisingly
high. Such sensitivity will be influenced by several factors.
For example, as the absorptance spectrum of a visual pigment
is influenced by pigment density, the degree of UV sensitivity
will depend in part on the length of a species’ outer segments
and the presence of a tapetum (which would effectively double
the pathlength of the outer segment). Furthermore, the nature
of the interactions between the different photoreceptor types at
short wavelengths and the effectiveness of short wavelengths
at triggering the transduction cascade, neither of which are
known, will also influence the degree of shortwave sensitivity.
(d) Function of ultraviolet sensitivity in mammals
It is tempting to seek a specific function for UV sensitivity,
although similar questions are rarely asked about other
parts of the spectrum. The functions proposed include;
mate choice, ‘secret’ intraspecific communication, navigation,
prey detection and foraging. However, UV light is little
different from other parts of the spectrum and its perception
need have no specific function beyond simply extending the
spectral range of the animal and improving its sensitivity.
Indeed, although UV has a role to play in both foraging
and mate choice in birds, longer wavelengths have been
shown to be more important [70,71]. Although in some
instances, UV may have a specific function, such as increas-
ing the visibility of the white fur of predatory polar bears
within a snowy landscape for reindeer [34] or enhancing
the visibility of urine trails for rodents [15,16], UV is normally
just a part of a wider spectrum of wavelengths all of which
are important for an animal’s behaviour.
Perhaps, the reason why there is a tendency to attribute
some special importance to UV sensitivity is simply that
humans are not able to see it [72].
(e) What is the function of preventing ultraviolet
radiation from reaching the retina?
Shortwave-sensitive visual pigments come in two forms:
violet-sensitive or UV-sensitive (UVS). Molecular evidence
suggests the UVS visual pigments are the ancestral form
[73]. Logically therefore, UV-transmitting lenses are also
ancestral and animals must have been subjected to selective
pressure to lose both UVS visual pigments and UV lens trans-
mission. Therefore, rather than seeking a specific function for
UV vision in mammals, it might be more pertinent to ask,
what is the function of animals having lenses that prevent
short wavelengths reaching the retina? Blocking UV could
be either protective or an aid to spatial resolution [42].
These different functions are by no means mutually exclusive
and both would explain the presence of UV-absorbing lenses
in mainly diurnal animals.
Removing short wavelengths, especially in long-lived
diurnal species, could protect the retina as the degree of reti-
nal light damage is considerably increased at shorter
wavelengths [74]. There is some experimental evidence for
such a function. For example, when the UV-absorbing
lenses of grey squirrels were removed, the retinae of these
eyes suffered more retinal damage than intact companion
eyes [75]. It has therefore been suggested that the reason noc-
turnal rodents, for example, can have UV-sensitive visual
pigments (and a UV-transparent lens) is that they are rela-
tively short-lived and habitually exposed to low light levels.
However, the lens cannot have a protective role in all species.
The reindeer, for example, lives in an extremely UV-rich
environment and can reach ages of up to 20 years, yet it
seems to suffer no ill effects from allowing UV to reach the
retina [34]. Similarly, some UV-sensitive parrots can live to
be over 50 years old with no apparent damage [76]. Either
species such as reindeer and parrots have mechanisms
to prevent the harmful effects of UV, or some species are
particularly sensitive to its deleterious consequences.
Short-wave absorbing filters will also increase image
quality as both the degree of Rayleigh scatter and chromatic
aberration are increased in this part of the spectrum [52],
although such a function is difficult to prove experimentally.
Interestingly, species such as diurnal primates and sciurid
rodents, whose lenses do remove short wavelengths, either
have a large proportion of cones (more than 20%) within
the retina and/or areas of very high cone density (more
than 100 000 cones mm
22
; see the electronic supplementary
material, table S5), which is consistent with a function of
such filters being to increase image quality. Interestingly,
the same argument has very recently been suggested to
account for the UV-absorbing ocular media of diurnal rap-
tors, which have extremely high visual acuity to facilitate
the capture of moving prey on the wing [77].
For species active that are at night, on the other hand,
the primary visual requirement is high absolute sensitivity
rather than spatial acuity, which will be facilitated by a
UV-transparent lens. Such animals generally have a lower
rspb.royalsocietypublishing.org Proc. R. Soc. B 281: 20132995
6

proportion of cones in their retina and no areas of increased
cone density, but often have areas of increased rod density
consistent with maximizing absolute sensitivity (see the
electronic supplementary material, table S5).
(f) Size(age)-related changes in lens transmission
It is not possible to characterize the spectral transmission of a
species’ lens by a single curve, as it will inevitably change as
a function of lens size. In some species, such as man, the lens
grows throughout life [78], and its size can be used to age the
animal [79]. In other species, lens growth levels off in older ani-
mals [80]. Generally, as shown by the four species in this study
for whom a range of lens sizes were available (P. livingstonii,
R. rattus,M. musculus and S. suricatta), the relative transmission
of short wavelengths decreases with increased lens size and
age (figure 4).
Some age-related change in lens transmission is an inevi-
table consequence of increased pathlength in older animals.
An approximate indication of the effect of lens size on
spectral transmission can be obtained by squaring the trans-
mission spectrum of a small lens to give a theoretical curve
for a lens twice the diameter [81,82]. For both the rat
(figure 4b) and mouse (data not shown), increased size is
insufficient to account for the decreased transmission
observed. The causes for the frequently described age-related
yellowing of the lens of primates [5,83] are complex [78] but
are in part the result of the attachment of the major
tryptophan-derived, short-wave absorbing lens pigment
(see the electronic supplementary material, S4) to lens pro-
teins [47,84]. The proximate causes of the decreased
shortwave transmission in other species, for example those
described here, that cannot be the result of a simple increase
in pathlength, are unclear.
It seems likely that such age-related changes in lens trans-
mission are the inevitable result of both increased lens size
and light exposure. Nonetheless, they might protect the
retina of older animals from the harmful UV radiation and,
for example, slow the rate of photoreceptor loss.
Acknowledgements. We are grateful to the following who helped in the
procurement of eyes: Stewart Thompson (Imperial College, University
of London); Ilse Pedler (Mercer and Hughes Veterinary practice, Saf-
fron Walden); Jim Bowmaker and Astrid Limb (University College
London); Margaret Stafford and John Lawrenson (City University
London); Wendy Steel (Royal Veterinary College, Potters Bar); Clare
Brazill-Adams (MRC National Institute for Medical Research, Mill
Hill); the Horniman Museum (London), Edmund Flach and Belinda
Clark (Zoological Society of London); Kellie Wyatt, Adina Valentine,
Christoph Schwitzer and Michelle Barrow (Bristol Zoo); Helen
Schwantje and Caite Nelson (Fish, Wildlife and Habitat Management
Branch state government BC, Canada). Especial thanks to Andrea
Bowden (ne
´e Thorpe) for allowing use of some unpublished data
from her PhD. Professors Julian Partridge, Roger Truscott, Leo Peichl
and Martin Glo
¨smann are thanked for helpful discussion.
Funding statement. G.J. was supported by the BBSRC for some of this
work.
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