Vole Urine Research Articles

Glareosin: a novel sexually dimorphic urinary lipocalin in the bank vole, Myodes glareolus.

The urine of bank voles (Myodes glareolus) contains substantial quantities of a small protein that is expressed at much higher levels in males than females, and at higher levels in males in the breeding season. This protein was purified and completely sequenced at the protein level by mass spectrometry. Leucine/isoleucine ambiguity was completely resolved by metabolic labelling, monitoring the incorporation of dietary deuterated leucine into specific sites in the protein. The predicted mass of the sequenced protein was exactly consonant with the mass of the protein measured in bank vole urine samples, correcting for the formation of two disulfide bonds. The sequence of the protein revealed that it was a lipocalin related to aphrodisin and other odorant-binding proteins (OBPs), but differed from all OBPs previously described. The pattern of secretion in urine used for scent marking by male bank voles, and the similarity to other lipocalins used as chemical signals in rodents, suggest that this protein plays a role in male sexual and/or competitive communication. We propose the name glareosin for this novel protein to reflect the origin of the protein and to emphasize the distinction from known OBPs.

Puumala hantavirus infection alters the odour attractiveness of its reservoir host.

The random-mixing assumptions of many parasite-transmission models are challenged if healthy individuals can alter their behaviour to reduce their risk of infection. Some pathogens reduce the attractiveness of their hosts' excretions, for example, potentially altering contact rates and thus the predicted force of infection for pathogens transmissible by contact with excretions. For bank voles (Myodes glareolus), contact with contaminated urine is an important route of transmission for Puumala hantavirus (PUUV); however, it is not known whether PUUV infection changes the voles' urinary odours or their attractiveness. Here, we use a Y-maze to test whether PUUV infection alters the attractiveness of male bank voles' urine. We presented wild-caught PUUV-free male and female bank voles with PUUV-infected conspecific urine, uninfected urine and a water control, and measured the relative and absolute latency to first visit, number of visits, and total time bank voles spent investigating each treatment over 30 min. PUUV infection significantly altered the bank voles' initial response to conspecific urine, with fewer visits and less time spent close to infected urine relative to uninfected urine, and less total time spent near the infected urine than the uninfected urine or control. These strong preferences weakened over the 30-min trial, however, partly due to a general decline in male activity, and there were no absolute differences between the treatments overall. This suggests that PUUV infection does change the attractiveness of bank vole urine to conspecifics, and we discuss the implications of these results for random-mixing assumptions.

PARADOX OF UV VISION IN RAPTORS RESOLVED

Unlike humans, most birds have photoreceptor pigments that are sensitive to ultraviolet (UV) light, which has short wavelengths of 300–400 nm. However, for raptors such as kestrels, the purpose of this UV vision has remained elusive and puzzling. Over 15 years ago, when scientists found that the urine from Finnish voles reflected UV light, it seemed the mystery had been solved – UV vision was useful for scouting out good hunting grounds based on the abundance of UV-reflecting pee. However, 10 years later, studies suggest that the raptors' UV pigments are almost insensitive to UV and at best only detect UV light with longer wavelengths nearer 400 nm. Instead of benefiting raptor predators, UV light might be of more use to another type of prey, songbirds. These small birds have UV pigments sensitive to short wavelengths as well as UV-reflecting plumage. If raptors are truly insensitive to UV, then songbirds can use their feathers to secretly communicate with other songbirds. But are the raptors completely unaware of these UV signals or can they still use UV for hunting? With this controversy unsolved, Olle Lind, a post-doc in Almut Kelber's lab at Lund University, Sweden, decided to investigate with the help of two PhD students, Mindaugas Mitkus and Peter Olsson (p. 1819).Lind realised that a missing key in this puzzle was that no one knew what wavelengths of light make it to the raptors' retinas: ‘Even before the light hits the retina, it's filtered through the cornea, the lens and the fluids within the eye. The whole ocular media acts as a cut-off filter and sets UV sensitivity automatically – if you can't get it [UV] to the retina, you won't be able to detect it!’ says Lind. Using eyes from euthanised raptors, the team measured how much UV was getting through the ocular media: ‘we excised the eye and then took away a piece from the back of the eye. We were then able to shine light through the eye, which wasn't stopped by the retina and at the back of the eye we had a probe instead’, explains Lind. They found that raptor eyes cut out a lot of UV light, with only UV light of higher wavelengths making it through to the retina. In one raptor, the red kite, most of the UV reaching the retina had a wavelength higher than 394 nm.So, perhaps vole urine reflects UV light with higher wavelengths? To test this, the team collected urine from voles they had trapped in the surrounding countryside, and measured how much UV light the urine reflected – but it didn't. Lind admits that he was not entirely surprised – many other studies have characterised mammalian urine and found that it does not reflect UV. However, knowing the sensitivity of the raptor's pigments and using his newly collected measurements – UV transmittance to the retina and UV reflectance from vole urine – Lind was able to model whether vole urine can be informative in some way to raptors. He concludes: ‘there is definitely no information in the UV, they can't use UV to find vole urine – at least not with Swedish voles!’So what about songbirds? Is enough UV light getting to the retina for the raptors to eavesdrop on communicating songbirds? Using previously collected data characterising UV reflectance of songbirds' plumage and their raptor-eye model, Lind says, ‘UV markings are not invisible to raptors; they can see them, but they might not be as conspicuous to them as they are to songbirds.’ So it would seem that raptors are neither blind nor highly sensitive to UV, and the question still remains – what are these UV-sensitive pigments doing in raptors?

Ultraviolet sensitivity and colour vision in raptor foraging

Raptors have excellent vision, yet it is unclear how they use colour information. It has been suggested that raptors use ultraviolet (UV) reflections from vole urine to find good hunting grounds. In contrast, UV plumage colours in songbirds such as blue tits are assumed to be 'hidden' communication signals, inconspicuous to raptors. This ambiguity results from a lack of knowledge about raptor ocular media transmittance, which sets the limit for UV sensitivity. We measured ocular media transmittance in common buzzards (Buteo buteo), sparrowhawks (Accipiter nisus), red kites (Milvus milvus) and kestrels (Falco tinnunculus) so that, for the first time, raptor UV sensitivity can be fully described. With this information, and new measurements of vole urine reflectance, we show that (i) vole urine is unlikely to provide a reliable visual signal to hunting raptors and (ii) blue tit plumage colours are more contrasting to blue tits than to sparrowhawks because of UV reflectance. However, as the difference between blue tit and sparrowhawk vision is subtle, we suggest that behavioural data are needed to fully resolve this issue. UV cues are of little or no importance to raptors in both vole and songbird interactions and the role of colour vision in raptor foraging remains unclear.

Consumption of grass endophytes alters the ultraviolet spectrum of vole urine

Fungal endophytes of grasses are known to benefit their hosts directly by increasing resistance to herbivores through mycotoxins. We propose and test assumptions of a novel hypothesis according to which fungal endophytes of grasses may benefit their hosts also indirectly by increasing the conspicuousness of a mammalian herbivore, the field vole (Microtus agrestis), to its avian predators by enhancing the ultraviolet visibility of vole urine. We found that field voles feeding on endophyte-infected meadow ryegrass (Lolium pratense) lost body mass, while voles feeding on non-infected meadow ryegrass gained mass. More interestingly, the maximum peak intensity of ultraviolet fluorescence in the urine of voles feeding on endophyte-infected grass shifted from over 380 nm to circa 370 nm, which is the suggested maximum sensitivity of the ultraviolet pigments in the eyes of vole-eating raptors. Therefore, grazing on endophyte-infected grass alters the ultraviolet spectrum of vole urine, thus potentially enhancing its visibility to avian predators.

Innate and learned aspects of vole urine UV-reflectance use in the hunting behaviour of the common kestrel Falco tinnunculus

Innate and learned aspects of vole urine UV-reflectance use in the hunting behaviour of the common kestrel Falco tinnunculus

Innate and learned aspects of vole urine UV‐reflectance use in the hunting behaviour of the common kestrel Falco tinnunculus

Some birds are known to use the UV reflectance in their feeding strategy. Knowing that the common kestrel Falco tinnunculus is able to recognise vole trails by perceiving the UV reflectance of their scent marks, this study was designed to investigate whether the use of scent marks in the UV range has an innate component, or if it is only acquired with experience. We tested the preference of 44 experienced adult and 49 naïve juvenile common kestrels in four types of arenas: (1) scent‐marked and covered with a UV transmitting filter (UV+SC), (2) scent‐marked and covered with a UV blocking filter (UV‐SC), (3) sprinkled with water and covered with a UV transmitting filter (UV+W), and (4) sprinkled with water and covered with a UV blocking filter (UV‐W). We assessed the birds’ preference by counting the number of visual scans and visits to each arena. The distribution of scans differed from random in both adults and juveniles. The birds scanned the UV+SC arena more often than the others. Since naïve individuals showed the same preference as experienced ones, we hypothesised that the association between vole scent UV reflectance and vole presence has an innate component in the common kestrel. Nevertheless, adults differed from juveniles because they perceived the scented arenas from the water sprinkled ones, in fact, adults scanned the UV‐SC arena more frequently than both UV+W and UV‐W arenas. This result suggests that the ability of detecting UV cues has a learned component.

NMR spectroscopy based metabonomic studies on the comparative biochemistry of the kidney and urine of the bank vole ( Clethrionomys glareolus), wood mouse ( Apodemus sylvaticus), white toothed shrew ( Crocidura suaveolens) and the laboratory rat

The metabolic profiles of three wild mammals that vary in their trophic strategies, the herbivorous bank vole ( Clethrionomys glareolus), the granivorous wood mouse ( Apodemus sylvaticus), and the insectivorous white-toothed shrew ( Crocidura suaveolens), were compared with that of a widely used strain of laboratory rat (Sprague Dawley). In conjunction with NMR spectroscopic investigations into the urine and blood plasma composition for these mammals, high resolution magic angle spinning (HRMAS) 1H-nuclear magnetic resonance (NMR) spectroscopy was applied to investigate the composition of intact kidney samples. Adaptation to natural diet affects both renal metabolism and urinary profiles, and while these techniques have been used to study the metabolism of the laboratory rat little is known about wild small mammals. The species were readily separated by their urinary profiles using either crude metabolite ratios or statistical pattern recognition. Bank vole urine contained higher concentrations of aromatic amino acids compared with the other small mammals, while the laboratory rats produced relatively more hippurate. HRMAS 1H-NMR demonstrated striking differences in both lipid concentration and composition between the wild mammals and Sprague Dawley rats. Bank voles contained high concentrations of the aromatic amino acids phenylalanine, tyrosine and tryptophan in all tissue and biofluids studied. This study demonstrates the analytical power of combined NMR techniques for the study of inter-species metabolism and further demonstrates that metabolic data acquired on laboratory animals cannot be extended to wild species.

Ultraviolet cues affect the foraging behaviour of blue tits

The function of avian ultraviolet (UV) vision is only just beginning to be understood. One plausible hypothesis is that UV vision enhances the foraging ability of birds. To test this, we carried out behavioural experiments using wild–caught blue tits foraging for cabbage moth and winter moth caterpillars on natural and artificial backgrounds. The light environment in our experiments was manipulated using either UV–blocking or UV–transmitting filters. We found that the blue tits tended to find the first prey item (out of four) more quickly when UV cues were present. This suggests that UV vision offers benefits to birds when searching for cryptic prey, despite the prey and backgrounds reflecting relatively little UV. Although there was no direct effect of UV on the time taken to find all four prey items in a trial, search performance in the absence of UV wavelengths tended to increase over the course of an experiment. This may reflect changes in the search tactics of the birds. To our knowledge, these are the first data to suggest that birds use UV cues to detect cryptic insect prey, and have implications for our understanding of protective coloration.

Do Tengmalm's owls see vole scent marks visible in ultraviolet light?

Scent markings (urine and faeces) of small mammals are visible in ultraviolet (UV) light. Diurnal kestrels,Falco tinnunculususe them as a cue to find areas of food abundance. We studied whether vole-eating, nocturnal Tengmalm's owls,Aegolius funereuscan see vole scent marks using UV-vision. In a laboratory experiment, 14 young (less than 6 months old) and 14 adult (more than 6 months old) owls were individually given a choice between four adjacent arenas: (1) an arena with vole urine and faeces in UV light; (2) an arena with vole urine and faeces in visible light; (3) a clean arena in UV light; and (4) a clean arena in visible light. Owls did not prefer any of the four arenas. Our results suggest that Tengmalm's owls probably do not use UV light as a cue to detect vole scent marks.

Attraction of kestrels to vole scent marks visible in ultraviolet light

IN northern Europe, broad four-year oscillations in small rodent and raptor populations are synchronous over hundreds of square kilometers1–6. Crashes in vole populations can induce wide emigration (> 1,000 km) of their predators7 –9, but almost nothing is known about how predators rapidly detect areas of vole abundance. Here we report on laboratory and field experiments on voles (Microtus agrestis) and kestrels (Falco tinnunculus). Voles mark their runaways with urine and faeces, which are visible in ultraviolet light. Wild kestrels brought into captivity were able to detect vole scent marks in ultraviolet light but not in visible light. In the field, kestrels hunted preferentially near experimental nest-boxes where artificial trails were treated with vole urine and faeces. We suggest that kestrels flying over an area can see and use vole scent marks to assess vole numbers. This ability would enable kestrels to 'screen' large areas in a relatively short time. Our results provide a novel explanation for how raptors detect patches of high vole densities without prior knowledge of local food resources.

Male Vole Urine Changes Luteinizing Hormone-Releasing Hormone and Norepinephrine in Female Olfactory Bulb

Female prairie voles (Microtus ochrogaster) exposed to a single drop of male urine on the upper lip showed changes in concentrations of luteinizing hormone-releasing hormone (LHRH) and norepinephrine in olfactory bulb tissue; no such changes occurred in dopamine concentration. The changes were measured in the posterior but not the anterior olfactory bulb tissue of females within 1 hour after they were exposed to urine. These females also showed rapid increases in serum concentrations of luteinizing hormone. Females exposed to water on the upper lip showed none of these changes. These results suggest that in this species LHRH and norepinephrine in the olfactory bulb may mediate luteinizing hormone release in response to external (pheromonal) chemical cues.