European Journal of Wildlife Research

, Volume 58, Issue 5, pp 811–819 | Cite as

Cone opsins and response of female chamois (Rupicapra rupicapra) to differently coloured raincoats

  • S. RavehEmail author
  • W. F. D. van Dongen
  • C. Grimm
  • P. Ingold
Original Paper


Alpine species are often exposed to intense levels of human recreational activities. Exactly how human disturbances influence the behaviour of these species is still open to much debate. For example, little is known regarding how the colourful clothing often worn by tourists influences the behaviour of animals. Tourists wearing colourful clothing may be more conspicuous to local wildlife and thus cause more disturbances. We therefore investigated this question in female chamois (Rupicapra rupicapra) in the Swiss Alps. We firstly investigated, via a morphological and an immunohistochemical approach, whether chamois are likely to have colour vision and would therefore be more likely to respond to different coloured clothing. We detected evidence of two cone types—short-wavelength-sensitive cones (S-cones, JH 455) and middle-wavelength-sensitive cones (M-cones, JH492) in the chamois retina—suggesting that chamois have dichromatic vision, similar to other ungulates. Secondly, via behavioural assays where a person wearing one of three coloured coats commonly worn by tourists (red, yellow and blue) approached a female chamois, we show that neither the alert and flight initiation distance nor the site of refuge were influenced by the raincoat colour. In addition, behavioural responses of the chamois were neither influenced by animal group size nor the presence of kids nor the time of the experiment. The results suggest that, although chamois possess colour vision, they do not react more strongly towards conspicuous colours worn by hikers. We discuss our results in light of what is already known about chamois biology and suggest implications for future studies.


Tourism Alert distance Flight initiation distance Clothing Colour vision Chamois Rupicapra rupicapra 



We thank the Canton Bern and the Jagdinspektorat for generously providing the hunting lodge and the Jagdinspektor P. Juesy and the gamekeepers R. Fuchs and P. Schwendimann for providing the eyes of the chamois. Furthermore, we thank the Bern University Hospital Department of Veterinary Medicine, M. Stoffel and his team for providing chemical additives, as well as K. Bennmann for the demonstration of eye enucleation. Thanks to Prof. Charlotte Remé (Dr. Med) and Andreas Wenzel (Dr. sc. nat.) of the Department of Ophthalmology, University of Zurich for the examination of the chamois retinas and their suggestions for this paper and also to Jeremy Nathans (Johns Hopkins, Baltimore, USA) for generously supplying the primary antibodies. We are grateful to J.-P. Airoldi's statistical help, as well as to C. Raaflaub, A. Imhasly, P. Enggist, T. Karels, R. Bergmüller, S. Kenyon, A. Nesterova and the AEN team's comments on the manuscript.


  1. Albrecht L (1988) Habituation von Gemsen Rupicapra rupicapra an den Menschen. Master. University of Zurich, SwitzerlandGoogle Scholar
  2. Arlettaz R, Patthey P, Baltic M, Leu T, Schaub M, Palme R, Jenni-Eiermann S (2007) Spreading free-riding snow sports represent a novel serious threat for wildlife. Proc R Soc Lond B Biol Sci 274:1219–1224CrossRefGoogle Scholar
  3. Arrese CA, Hart NS, Thomas N, Beazley LD, Shand J (2003a) Trichomacy in Australian marsupials. Curr Biol 12:657–660CrossRefGoogle Scholar
  4. Arrese CA, Rodger J, Beazley LD, Shand J (2003b) Topographies of retinal cone photoreceptors in two Australian marsupials. Visual Neurosci 20:307–311CrossRefGoogle Scholar
  5. Bäbler R (2001) Beeinflussen Jagd und Tourismus die Reaktionsempfindlichkeit von Gemsen (Rupicapra rupicapra)? Master. University of Bern, SwitzerlandGoogle Scholar
  6. Bellairs R, Harkness ML, Harkness RD (1975) The structure of the tapetum of the eye of the sheep. Cell Tissue Res 157:73–91PubMedCrossRefGoogle Scholar
  7. Bellman KL, Krasne FB (1983) Adaptive complexity of interactions between feeding and escape in crayfish. Science 221:779–781PubMedCrossRefGoogle Scholar
  8. Birgersson B, Alm U, Forkman B (2001) Colour vision in fallow deer: a behavioural study. Anim Behav 61:367–371CrossRefGoogle Scholar
  9. Blanks JC, Johnson LV (1984) Specific binding of peanut lectin to a class of retinal photoreceptor cells: a species comparison. Invest Ophthalmol Vis Sci 25:546–557PubMedGoogle Scholar
  10. Carroll J, Murphy CJ, Neitz M, Ver Hoeve JN, Neitz J (2001) Photopigment basis for dichromatic colour vision in the horse. J of vision 1:80–87Google Scholar
  11. Cederna A, Lovari S (1985) The impact of tourism on chamois feeding activities in an area of the Abruzzo National Park, Italy. In: Lovari S (ed) The biology and management of mountain ungulates. T Croom Helm, LondonGoogle Scholar
  12. Chiu MI, Nathans J (1994) Blue cones and cone bipolar cells share transcriptional specificity as determined by expression of human blue visual pigment-derived transgenes. J Neurosci 14:3426–3436PubMedGoogle Scholar
  13. Cooper WE (2000) Tradeoffs between predation risk and feeding in a lizard, the broad-headed skink (Eumeces laticeps). Behaviour 137:1175–1189CrossRefGoogle Scholar
  14. Cooper WE Jr, Pérez-Mellado V, Baird T, Baird TA, Caldwell JP, Vitt LJ (2003) Effects of risk, cost, and their interaction on optimal escape by nonrefuging Bonaire whiptail lizards, Cnemidophorus murinus. Behav Ecol 14:288–293CrossRefGoogle Scholar
  15. Dalmau A, Ferret A, Manteca X (2010) Vigilance behavior of Pyrenean chamois Rupicapra pyrenaica pyrenaica: effect of sex and position in the herd. Curr Zool 56:232–237Google Scholar
  16. Dkhissi-Benyahya O, Szel A, Degrip WJ, Cooper HM (2001) Short and mid-wavelength cone distribution in a nocturnal strepsirrhine primate (Microcebus murinus). J Comp Neurol 438:490–504PubMedCrossRefGoogle Scholar
  17. Doucet SM, Mennill DJ, Hill GE (2007) The evolution of signal design in manakin plumage ornaments. Amer Nat 169:S62–S80CrossRefGoogle Scholar
  18. Endler JA (1993) The color of light in forests and its implications. Ecol Monogr 63:1–27CrossRefGoogle Scholar
  19. Enggist-Düblin P, Ingold P (2003) Modelling the impact of different forms of wildlife harassment, exemplified by a quantitative comparison of the effects of hikers and paragliders on feeding and space use of chamois Rupicapra r. rupicapra. Wildlife Biol 1:37–45Google Scholar
  20. Frid A (2003) Dall's sheep response to overflights by helicopter and fixed-wing aircraft. Biol Conserv 110:387–399CrossRefGoogle Scholar
  21. Gander H, Ingold P (1997) Reactions of male alpine chamois Rupicapra r. rupicapra to hikers, joggers and mountainbikers. Biol Conserv 9:107–109CrossRefGoogle Scholar
  22. Glosmann M, Ahnelt PK (2002) A mouse-like retinal cone phenotype in the Syrian hamster: S opsin coexpressed with M opsin in a common cone photoreceptor. Brain Res 929:139–146PubMedCrossRefGoogle Scholar
  23. Hack I, Peichl L (1999) Horizontal cells of the rabbit retina are non-selectively connected to the cones. Eur J Neurosci 11:2261–2274PubMedCrossRefGoogle Scholar
  24. Hageman GS, Johnson LV (1986) Biochemical characterization of the major peanut-agglutinin-binding glycoproteins in vertebrate retinae. J Comp Neurol 249(499–510):482–483Google Scholar
  25. Hamr J (1988) Disturbance behaviour of chamois in an alpine tourist area of Austria. Mt Res Dev 8:65–73CrossRefGoogle Scholar
  26. Harkin EL, van Dongen WFD, Herberstein ME, Elgar MA (2000) The influence of visual obstructions on the vigilance and escape behaviour of house sparrows, Passer domesticus. Aust J Zool 48:259–263CrossRefGoogle Scholar
  27. Hemmi JM, Grünert U (1999) Distribution of photoreceptors types in the retina of a marsupial, the tammar wallaby (Macropus eugenii). Vis Neurosci 16:291–302PubMedCrossRefGoogle Scholar
  28. Hicks LL, Elder JM (1979) Human disturbance of Sierra Nevada bighorn sheep. J Wildlife Manage 43:909–915CrossRefGoogle Scholar
  29. Hüppop O (1995) Störungsbewertung anhand physiologischer Parameter. Ornithologischer Beobachter 92:257–268Google Scholar
  30. Ingold P (2005) Freizeitaktivitäten im Lebensraum der Alpentiere: Konfliktbereiche zwischen Mensch und Tier. Mit einem Ratgeber für die Praxis, Haupt, VerlagGoogle Scholar
  31. Ingold P, Pfister U, Baechler E, Enggist-Dueblin P (1998) Pattern and rhythm of activity in alpine chamois Rupicapra r. rupicapra during winter. Z. Säugetierkd 63:183–185Google Scholar
  32. Jacobs GH (1981) Comparative colour vision. Academic Press, New YorkGoogle Scholar
  33. Jacobs GH (1993) The distribution and nature of colour vision among the mammals. Biol Rev 68:413–471PubMedCrossRefGoogle Scholar
  34. Jacobs GH (2009) Evolution of colour vision in mammals. Philos Trans R Soc Lond B Biol Sci 364:2957–2967PubMedCrossRefGoogle Scholar
  35. Jacobs GH, Deegan JF II, Crognale MA, Femwick JA (1993) Photopigments of dogs and foxes and their implications for canid vision. Vis Neurosci 10:173–180PubMedCrossRefGoogle Scholar
  36. Jacobs GH, Deegan JF II, Neitz J, Murphy BP, Miller KV, Marchinton RL (1994) Electrophysiological measurements of spectral mechanisms in the retina of two cervids: white-tailed deer (Odocoileus virginianus) and fallow deer (Dama dama). J Comp Neurol 174:551–557Google Scholar
  37. Jacobs GH, Deegan JF II, Neitz J (1998) Photopigment basis for dichromatic colour vision in cows, goats, and sheep. Vis Neurosci 15:581–584PubMedCrossRefGoogle Scholar
  38. Kaskan PM, Franco ECS, Yamada ES, Silveira LC, Darlington RB, Finlay BL (2005) Peripheral variability and central constancy in mammalian visual system evolution. Proc R Soc B 272:91–100PubMedCrossRefGoogle Scholar
  39. Keller V (2001) Schutzzonen für Wasservögel-Grundsätze und Erfahrungen aus der Schweiz. Laufener Seminarbeiträge 1(01):83–86Google Scholar
  40. Klose S, Welbergen J, Goldizen A, Kalko E (2009) Spatio-temporal vigilance architecture of an Australian flying-fox colony. Behav Ecol Sociobiol 63:371–380CrossRefGoogle Scholar
  41. Koba Y, Tanida H (1999) How do miniature pigs discriminate between people? The effect of exchanging cues between a non-handler and their familiar handler on discrimination. Appl Anim Behav Sci 61:239–252CrossRefGoogle Scholar
  42. Kobelt M (2004) Reactions of alpine chamois Rupicapra rup. rupicapra to human voices. Master. University of Bern, SwitzerlandGoogle Scholar
  43. Krause J, Godin JGJ (1996) Influence of prey foraging posture on flight behavior and predation risk: predators take advantage of unwary prey. Behav Ecol 7:264–271Google Scholar
  44. Krishnamoorthy V, Jain V, Cherukuri P, Baloni S, Dhingra NK (2008) Intravitreal injection of fluorochrome-conjugated peanut agglutinin results in specific and reversible labeling of mammalian cones in vivo. Invest Ophthalmol Vis Sci 49:2643–2650PubMedCrossRefGoogle Scholar
  45. MacArthur RA, Geist V, Johnston RH (1982) Cardiac and behavioural responses if mountain sheep to human disturbance. J Wildlife Manage 46:351–358CrossRefGoogle Scholar
  46. Mainini B, Neuhaus P, Ingold P (1993) Behaviour of marmots Marmota marmota under the influence of different hiking activities. Biol Conserv 64:161–164CrossRefGoogle Scholar
  47. Marbacher H (1989) Soziale Organisation und Konkurrenz in einer Herde von jungeführenden Gemsgeissen Rupicapra rupicapra. Master. University of Bern, SwitzerlandGoogle Scholar
  48. Martin PR, Grünert U (1999) Analysis of the short-wavelength sensitive (“blue”) cone mosaic in the primate retina: comparison New World and Old World monkeys. J Comp Neurol 406:1–14PubMedCrossRefGoogle Scholar
  49. Martinetto K, Cugnasse JM (2001) Reaction distance in Mediterranean Mouflon (Ovis gmelini musimon x Ovis sp.) in the presence of hikers with a dog on the Caroux plateau (Herault, France). Revue D Ecologie-la Terre Et La Vie 56:231–242Google Scholar
  50. Munkenbeck NW (1982) Colour vision in sheep. J Anim Sci 55(suppl1):129Google Scholar
  51. Naylor LM, Wisdom MJ, Anthony RG (2009) Behavioural responses of North American elk to recreational activity. J Wildlife Manage 73:328–338CrossRefGoogle Scholar
  52. Neumann W, Ericsson G, Dettki H (2010) Does off-trail backcountry skiing disturb moose? Eur J Wildlife Res 56:513–518CrossRefGoogle Scholar
  53. Ollivier FJ, Samuelson DA, Brooks DE, Lewis PA, Kallberg ME, Komáromy AM (2004) Comparative morphology of the tapetum lucidum (among selected species). Vet Ophthalmol 7:11–22PubMedCrossRefGoogle Scholar
  54. Patterson IJ (1988) Response of Apennine chamois to human disturbance. Z. Säugetierkd 53:245–252Google Scholar
  55. Reimers E, Eftestol S, Colman JE (2003) Behavior responses of wild reindeer to direct provocation by snowmobile or skier. J Wildlife Manage 67:747–754CrossRefGoogle Scholar
  56. Robbins CT (1993) Wildlife feeding and nutrition. 2nd ed. Academic Press, Inc. San Diego, CaliforniaGoogle Scholar
  57. Ruckstuhl KE, Ingold P (1998) Baby-sitting in chamois: a form of cooperation in females? Mammalia 62:125–128Google Scholar
  58. Sandmann D, Boycott BB, Peichl L (1996) Blue-cone horizontal cells in the retinae of horses and other Equidae. J Neurosci 16:3381–3396PubMedGoogle Scholar
  59. Schaal A, Boillet F (1992) Chamois and human disturbance in the Vosges mountains. In: Spitz, F., Janeau, G., Gonzalez, G., Aulanger (eds) Toulouse. Ongulés Ungulates 91, Proc. int. symp. S. 639-642.Google Scholar
  60. Schnidrig-Petrig R (1994) Modern icarus in wildlife habitat: effects of paraglidering on the behaviour, habitat use and body condition of chamois (Rupicapra r. rupicapra). Dissertation. University of Bern, SwitzerlandGoogle Scholar
  61. Schnidrig-Petrig R, Ingold P (2001) Effects of paragliding on chamois Rupicapra r. rupicapra. Wildlife Biol 7:285–294Google Scholar
  62. Schröder W, Elsner-Schack I (1985) Correct age determination in chamois. In: Lovari S (ed) Biology and management of mountain ungulates. Croom Helm, London, pp 65–70Google Scholar
  63. Scrimgeour GJ, Culp JM (1994) Feeding while evading predators by a lotic mayfly: linking short-term foraging behaviours to long-term fitness consequences. Oecologia 100:128–134CrossRefGoogle Scholar
  64. Siemers B, Backhaus W, Franz H (1999) Colour vision in farm animals: evidence for trichromacy in dwarf goats. Proceedings of the 27th neurobiology conference (Göttingen), Georg Thieme Verlag Stuttgart, NY.Google Scholar
  65. Stankowich T (2008) Ungulate flight responses to human disturbance: a review and meta-analysis. Biol Conserv 141:2159–2173CrossRefGoogle Scholar
  66. Stankowich T, Blumstein DT (2005) Fear in animals: a meta-analysis and review of risk assessment. Proc R Soc B 272:2627–2634PubMedCrossRefGoogle Scholar
  67. Taylor AR, Knight RL (2003) Wildlife responses to recreation and associated visitor perceptions. J Appl Ecol 13:951–963CrossRefGoogle Scholar
  68. Tyler NC (1991) Short-term behavioural responses of Svalbard reindeer Rangifer tarandus platyrhynchus to direct provocation by a snowmobile. Biol Conserv 56:179–194CrossRefGoogle Scholar
  69. Unoki K, Uehara F, Sameshima M, Nakano K, Ohba N (1988) Specific binding of peanut agglutinin to foveal and peripheral cone photoreceptors of monkey retina. Ophthalmic Res 20:112–116PubMedCrossRefGoogle Scholar
  70. Wikler KC, Szel A, Jacobsen AL (1996) Positional information and opsin identity in retinal cones. J Comp Neurol 374:96–107PubMedCrossRefGoogle Scholar
  71. Zeller R (1991) Zum Verhalten von Gemsgeissen unter dem Einfluss vonGoogle Scholar
  72. Zimmerli R (1993) Das Verhalten von Murmeltieren unter dem Einfluss eines unterschiedlich starken Wanderbetriebes: Aspekte der Nahrungsaufnahme und der Gebietsnutzung. Master. University of Bern, SwitzerlandGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • S. Raveh
    • 1
    • 2
    Email author
  • W. F. D. van Dongen
    • 2
  • C. Grimm
    • 3
  • P. Ingold
    • 1
  1. 1.Ethology and Nature Conservation, Department of ZoologyUniversity of BernBerneSwitzerland
  2. 2.Konrad Lorenz Institute of Ethology, Department of Integrative Biology and EvolutionUniversity of Veterinary MedicineViennaAustria
  3. 3.Lab for Retinal Cell Biology, Department of OphthalmologyUniversity of ZurichSchlierenSwitzerland

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