It is well known that avian predators can use prey excretions such as
urine and feces to track their prey, and the urine and feces of small mammalian
herbivores can reflect ultraviolet (UV) light and emit fluorescent light. There are still some debates as to whether UV visibility of small mammalian herbivores’ urine
is used as a hunting cue by avian raptors. Some studies in Europe have
demonstrated that diurnal raptors are capable of utilizing these cues to target
key prey species. However, researchers in Australia have argued that raptors do not use the UV visibility of urine
while hunting. To our knowledge, there are no reports from Asia
concerning the ultraviolet spectral characteristics of small mammal herbivores’ urine.
This study examined the UV spectral properties of urine from 6 small mammal
herbivores species by comparing the UV reflectance and fluorescence spectra of
urine from small mammalian herbivores living in plateau meadows, plateau
shrubs, open marshland, farmland, and semi-desert grassland in China. In
addition, we compared the UV spectral properties of urine from ground-dwelling
species of rodents and subterranean species
to determine whether ultraviolet visibility of small mammal herbivores’ urine
could be used as a visual signal by Asian vole-eating raptors. The results
showed that: 1) the SC370 values of urine from four small mammal herbivores species were ordered as plateau pika (plateau
meadow) > root voles (plateau bush) > reed voles (swampland) >
Brandt’s vole (desert grassland); and 2) UV
fluorescence peak intensity and
References
[1]
Anthony, D. A., Roger, P. P., Chris, D. et al. (2008). Livestock Grazing, Plateau Pikas, and the Conservation of Avian Biodiversity on the Tibetan Plateau. Biological Conservation, 141, 1972-1981. https://doi.org/10.1016/j.biocon.2008.05.010
[2]
Aschwanden, J., Birrer, S., & Jenni, L. (2005). Are Ecological Compensation Areas Attractive Hunting Sites for Common Kestrels (Falco tinnunculus) and Long-Eared Owls (Asio otus)? Journal of Ornithology, 146, 279-286. https://doi.org/10.1007/s10336-005-0090-9
[3]
Brown, R. E., & Macdonald, D. W. (1985). Social Odours in Mammals (pp. 121-127). Clarendon Press.
[4]
Chávez, A. E., Bozinovic, F., Peichl, L. et al. (2003). Retinal Spectral Sensitivity, Fur Coloration, and Urine Reflectance in the Genus Octodon (Rodentia): Implications for Visual Ecology. Investigative Ophthalmology & Visual Science, 44, 2290-2296. https://doi.org/10.1167/iovs.02-0670
[5]
Dai, X., Zhang, Y. Q., Jiang, L. Y. et al. (2014). Evaluation of the Variations in Secondary Metabolite Concentrations of Leymus chinensis Seedlings. Israel Journal of Ecol Ogy and Evolution, 60, 75-84. https://doi.org/10.1080/15659801.2014.986878
[6]
Desjardins, C., Maruniak, J., & Bronson, F. (1973). Social Rank in House Mice: Differentiation Revealed by Ultraviolet Visualization of Urinary Marking Patterns. Science, 182, 939-941. https://doi.org/10.1126/science.182.4115.939
[7]
Endler, J. A. (1993) The Color of Light in Forests and Its Implications. Ecological monographs, 63, 1-27. https://doi.org/10.2307/2937121
[8]
Fenn, M. G., & Macdonald, D. W. (1995). Use of Middens by Red Foxes: Risk Reverses Rhythms of Rats. Journal of Mammalogy, 76, 130-136. https://doi.org/10.2307/1382321
[9]
Goldsmith, T. H. (1990). Optimization, Constraint, and History in the Evolution of Eyes. Quarterly Review of Biology, 65, 281-322. https://doi.org/10.1086/416840
[10]
Halle, S. (1993). Pattern of Predation Risk in Microtine Rodents. Oikos, 68, 510-518. https://doi.org/10.2307/3544919
[11]
Härmä, O., Kareksela, S., Siitari, H. et al. (2011). Pygmy Owl Glaucidium passerinum and the Usage of Ultraviolet Cues of Prey. Journal of Avian Biology, 42, 89-91. https://doi.org/10.1111/j.1600-048X.2010.05192.x
[12]
Honkavaara, J., Koivula, M., Korpimäki, E. et al. (2002). Ultraviolet Vision and Foraging in Terrestrial Vertebrates. Oikos, 98, 505-511. https://doi.org/10.1034/j.1600-0706.2002.980315.x
[13]
Hughes, N. K., Price, C. J., & Banks, P. B. (2010). Predators Are Attracted to the Olfactory Signals of Prey. PLoS ONE, 5, e13114. https://doi.org/10.1371/journal.pone.0013114
[14]
Huitu, O., Helander, M., Lehtonen, P. et al. (2008). Consumption of Grass Endophytes Alters the Ultraviolet Spectrum of Vole Urine. Oecologica, 156, 333-340. https://doi.org/10.1007/s00442-008-0984-3
[15]
Hurst, J. L. (1990). Urine Marking in Populations of Wild House Mice Mus domesticus Rutty III. Communication between the Sexes. Animal Behavior, 40, 233-243. https://doi.org/10.1016/S0003-3472(05)80918-2
[16]
Janzen, D. H. (1980). When Is It Coevolution? Evolution, 34, 611-612. https://doi.org/10.1111/j.1558-5646.1980.tb04849.x
[17]
Johnsingh, A. (1992). Prey Selection in Three Large Sympatric Carnivores in Bandipur. Journal of Mammalogy, 56, 517-526. https://doi.org/10.1515/mamm.1992.56.4.517
[18]
Kellie, A., Dain, S. J., & Banks, P. B. (2004). Ultraviolet Properties of Australian Mammal Urine. Journal of Comparative Physiology, 190, 429-435. https://doi.org/10.1007/s00359-004-0507-6
[19]
Koivula, M., & Korpimäki, E. (2001). Do Scent Marks Increase Predation Risk of Microtine Rodents? Oikos, 95, 275-281. https://doi.org/10.1034/j.1600-0706.2001.950209.x
[20]
Koivula, M., & Viitala, J. (1999). Rough-Legged Buzzards Use Vole Scent Marks to Assess Hunting Areas. Journal of Avian Biology, 30, 329-332. https://doi.org/10.2307/3677362
[21]
Koivula, M., Korpimaki, E., & Viitala, J. (1997). Do Tengmalm’s Owls See Vole Scent Marks Visible in Ultraviolet Light? Animal Behavior, 54, 873-877. https://doi.org/10.1006/anbe.1996.0513
[22]
Koivula, M., Koskela, E., & Viitala, J. (1999). Sex and Age-Specific Differences in Ultraviolet Reflectance of Scent Marks of Bank Voles (Clethrionomys glareolus). Journal of Comparative Physiology A, 185, 561-564. https://doi.org/10.1007/s003590050416
[23]
Koivula, M., Viitala, J., & Korpimaki, E. (1999). Kestrels Prefer Scent Marks According to Species and Reproductive Status of Voles. écoscience, 6, 415-420. https://doi.org/10.1080/11956860.1999.11682544
[24]
Korpimäki, E., & Krebs, C. J. (1996). Predation and Population Cycles of Small Mammals. BioScience, 46, 754-764. https://doi.org/10.2307/1312851
[25]
Kullberg, C. (1995). Strategy of the Pygmy Owl While Hunting Avian and Mammalian Prey. Ornis Fennica, 7, 72-78.
[26]
Li, B., Wang, Y., Zhang, M. W. et al. (2008). Some Behavior of Microtus fortis calamorum during Migration While Population Outbreak in Dongting Lake Area. Chinese Journal of Zoology, 43, 57-63.
[27]
Lima, S. L. (1998). Stress and Decision-Making under the Risk of Predation: Recent Developments from Behavioral, Reproductive, and Ecological Perspectives. Advance in the Study Behavior, 27, 215-290. https://doi.org/10.1016/S0065-3454(08)60366-6
[28]
Lind, O., Mitkus, M., Olsson, P. et al. (2013). Ultraviolet Sensitivity and Colour Vision in Raptor Foraging. Journal of Experimental Biology, 216, 1819-1826. https://doi.org/10.1242/jeb.082834
[29]
Mappes, T., Halonen, M., Suhonen, J. et al. (1993). Selective Avian Predation on a Population of the Field Vole, Microtus agrestis: Greater Vulnerability of Males and Subordinates. Ethology Ecology & Evolution, 5, 519-527.
[30]
Norrdahl, K., & Korpimäki, E. (1993). Predation and Interspecific Competition in Two Microtus Voles. Oikos, 67, 149-158. https://doi.org/10.2307/3545105
[31]
Palme, R., Rettenbacher, S., Touma, C. et al. (2005). Stress Hormones in Mammals and Birds: Comparative Aspects Regarding Metabolism, Excretion, and Noninvasive Measurement in Fecal Samples. Annals of the New York Academy of Sciences, 1040, 162-171. https://doi.org/10.1196/annals.1327.021
[32]
Peichl, L., Chavez, A. E., Ocampo, A. et al. (2005). Eye and Vision in the Subterranean Rodent Cururo (Spalacopus cyanus, Octodontidae). Journal of Comparative Neurology, 486, 197-208. https://doi.org/10.1002/cne.20491
[33]
Probst, R., Pavlicev, M., & Viitala, J. (2002). UV Reflecting Vole Scent Marks Attract a Passerine, the Great Grey Shrike Lanius excubitor. Journal of Avian Biology, 33, 437-440. https://doi.org/10.1034/j.1600-048X.2002.02760.x
[34]
Qu, J. P., Li, W. J., Yang, M. et al. (2013). Life History of the Pika (Ochotona curzoniae) in Alpine Meadow of the Tibetan Plateau. Mammalian Biology, 78, 68-72. https://doi.org/10.1016/j.mambio.2012.09.005
[35]
Roger, P. P., Chris, D., Zhang, Y. M., & Lin, H. (2007). Population Dynamics and Responses to Management of Plateau Pikas (Ochotona curzoniae). Journal of Applied Ecology, 44, 615-624. https://doi.org/10.1111/j.1365-2664.2007.01287.x
[36]
Shao, Y., Li, J. X., Ge, R. L. et al. (2015). Genetic Adaptations of the Plateau Zokor in High-Elevation Burrows. Scientific Reports, 5, Article No. 17262. https://doi.org/10.1038/srep17262
[37]
Su, J. P. (2001). A Comparative Study on the Habitat Selection of Plateau Pika (Ochotona curzoniae) and Gansu Pika (Ochotona Cansus). Ph.D. Dissertation, the Chinese Academy of Sciences.
[38]
Trejo, A., & Guthmann, N. (2003). Owl Selection on Size and Sex Classes of Rodents: Activity and Microhabitat Use of Prey. Journal of Mammalogy, 84, 652-658. https://doi.org/10.1644/1545-1542(2003)084%3C0652:OSOSAS%3E2.0.CO;2
[39]
Viitala, J., Korplmäki, E., Palokangas, P. et al. (1995). Attraction of Kestrels to Vole Scent Marks Visible in Ultraviolet Light. Nature, 373, 425-427. https://doi.org/10.1038/373425a0
[40]
Wan, X. R., Liu, W., Wang, G. H. et al. (2006). Seasonal Changes of the Activity Patterns of Brandt’s Vole (Lasiopodomys brandtii) in the Typical Steppe in Inner Mongolia. Acta Theriology Sinica, 26, 226-234.
[41]
Wang, D. H., Sun, R. Y., Wang, Z. W. et al. (2013). Effects of Temperature and Photoperiod on Thermogenesis in Plateau Pikas (Ochotona curzoniae) and Root Voles (Microtus oeconomus). Mammalian Biology, 78, 68-72.
[42]
Zampiga, E., Gaibani, G., Csermely, D. et al. (2006). Innate and Learned Aspects of Vole Urine UV-Reflectance Use in the Hunting Behaviour of the Common Kestrel Falco tinnunculus. Journal of Avian Biology, 37, 318-322. https://doi.org/10.1111/j.2006.0908-8857.03825.x
[43]
Zhang, Z. B., Zhang, Y. M., & Liu, J. K. (2003). Burrowing Rodents as Ecosystem Engineers: The Ecology and Management of Plateau Zokors Myospalax fontanierii in Alpine Meadow Ecosystems on the Tibetan Plateau. Mammal Review, 33, 284-294. https://doi.org/10.1046/j.1365-2907.2003.00020.x
