Journal of Comparative Physiology A

, Volume 199, Issue 12, pp 1077–1092 | Cite as

Exploring the mammalian sensory space: co-operations and trade-offs among senses

  • Sirpa Nummela
  • Henry Pihlström
  • Kai Puolamäki
  • Mikael Fortelius
  • Simo Hemilä
  • Tom Reuter
Original Paper


The evolution of a particular sensory organ is often discussed with no consideration of the roles played by other senses. Here, we treat mammalian vision, olfaction and hearing as an interconnected whole, a three-dimensional sensory space, evolving in response to ecological challenges. Until now, there has been no quantitative method for estimating how much a particular animal invests in its different senses. We propose an anatomical measure based on sensory organ sizes. Dimensions of functional importance are defined and measured, and normalized in relation to animal mass. For 119 taxonomically and ecologically diverse species, we can define the position of the species in a three-dimensional sensory space. Thus, we can ask questions related to possible trade-off vs. co-operation among senses. More generally, our method allows morphologists to identify sensory organ combinations that are characteristic of particular ecological niches. After normalization for animal size, we note that arboreal mammals tend to have larger eyes and smaller noses than terrestrial mammals. On the other hand, we observe a strong correlation between eyes and ears, indicating that co-operation between vision and hearing is a general mammalian feature. For some groups of mammals we note a correlation, and possible co-operation between olfaction and whiskers.


Sensory ecology Vision Olfaction Hearing Vibrissae 



For access to scientific collections we thank: Hans J. Baagøe, Mogens Andersen, and Abdi Hedayat (Natural History Museum of Denmark, Copenhagen), Per Ericson and Olavi Grönwall (Swedish Museum of Natural History, Stockholm), Gerhard Storch (Senckenberg Research Institute, Frankfurt), and Ilpo K. Hanski and Martti Hildén (Finnish Museum of Natural History, Helsinki). We are grateful to Kristian Donner and Lotta Sundström for constructive criticism and valuable suggestions on earlier versions of this manuscript. We thank the handling editor Günther Zupanc, and three anonymous reviewers for help and advice with this manuscript. This project was supported by the Academy of Finland (SN, MF), Ella and Georg Ehrnrooth Foundation (HP), Oskar Öflund Foundation (HP), ALGODAN (KP), and the Finnish Society of Sciences and Letters (TR).

Supplementary material

359_2013_846_MOESM1_ESM.pdf (144 kb)
Supplementary material 1 (PDF 143 kb)


  1. Ahnelt PK, Kolb H (2000) The mammalian photoreceptor mosaic–adaptive design. Progr Retinal Eye Res 19:711–777Google Scholar
  2. Barlow HB (1981) The Ferrier Lecture, 1980. Critical limiting factors in the design of the eye and visual cortex. Proc R Soc Lond B 212:1–34PubMedGoogle Scholar
  3. Barlow HB, Mollon JD (eds) (1982) The senses. Cambridge University Press, London, pp 1–490Google Scholar
  4. Barth FG, Giampieri-Deutsch P, Klein H-D (eds) (2012) Sensory perception: mind and matter. Springer, Wien, pp 1–404Google Scholar
  5. Békésy G von (1960) Experiments in hearing. McGraw-Hill, New York, pp 1–745Google Scholar
  6. Bhatnagar KP, Kallen FC (1975) Quantitative observations on the nasal epithelia and olfactory innervation in bats. Acta Anat 91:272–282PubMedGoogle Scholar
  7. Bininda-Emonds ORP, Cardillo M, Jones KE, MacPhee RDE, Beck RMD, Grenyer R, Price SA, Vos RA, Gittleman JL, Purvis A (2007) The delayed rise of present-day mammals. Nature 446:507–512PubMedGoogle Scholar
  8. Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer Associates, Sunderland, pp 1–882Google Scholar
  9. Bruns V, Fiedler J, Kraus H-J (1983–1984) Structural diversity of the inner ear of bats. Myotis 21–22:52–61Google Scholar
  10. Burr D, Silva O, Cicchini GM, Banks MS, Morrone MC (2009) Temporal mechanisms of multimodal binding. Proc R Soc B 276:1761–1769PubMedGoogle Scholar
  11. Catania KC (2005) Evolution of sensory specializations in insectivores. Anat Rec A 287A:1038–1050Google Scholar
  12. Catania KC, Hare JF, Campbell KL (2008) Water shrews detect movement, shape, and smell to find prey underwater. Proc Natl Acad Sci USA 105:571–576PubMedGoogle Scholar
  13. Chandrasekaran C, Lemus L, Trubanova A, Gondan M, Ghazanfar AA (2011) Monkeys and humans share a common computation for face/voice integration. PLoS Comput Biol 7:e1002165PubMedGoogle Scholar
  14. Dalland JI (1965) Hearing sensitivity in bats. Science 150:1185–1186PubMedGoogle Scholar
  15. Darwin C (1859) On the origin of species. John Murray, London, pp 1–502Google Scholar
  16. Dehnhardt G, Mauck B (2008) The physics and physiology of mechanoreception. In: Thewissen JGM, Nummela S (eds) Sensory evolution on the threshold: adaptations in secondarily aquatic vertebrates. University of California Press, Berkeley, pp 287–293Google Scholar
  17. Dusenbery DB (1992) Sensory ecology: how organisms acquire and respond to information. W.F. Freeman and Company, New York, pp 1–558Google Scholar
  18. Eisthen HL, Schwenk K (2008) The chemical stimulus and its detection. In: Thewissen JGM, Nummela S (eds) Sensory evolution on the threshold: adaptations in secondarily aquatic vertebrates. University of California Press, Berkeley, pp 35–41Google Scholar
  19. Eronen J, Polly PD, Fred M, Damuth J, Frank DC, Mosbrugger V, Scheidegger C, Stenseth NC, Fortelius M (2010) Ecometrics: the traits that bind the past and present together. Integr Zool 5:88–101PubMedGoogle Scholar
  20. Evans EF (1982) Basic physics and psychophysics of sound. In: Barlow HB, Mollon JD (eds) The Senses. Cambridge University Press, Cambridge, pp 239–250Google Scholar
  21. Fay RR (1988) Hearing in vertebrates: a psychophysics databook. Hill-Fay Associates, Winnetka, pp 1–621Google Scholar
  22. Fay RR (1992) Structure and function in sound discrimination among vertebrates. In: Webster DB, Fay RR, Popper AN (eds) The evolutionary biology of hearing. Springer, New York, pp 229–263Google Scholar
  23. Fleischer G (1978) Evolutionary principles in the mammalian middle ear. Adv Anat Embryol Cell Biol 55:1–70Google Scholar
  24. Geisler CD (1998) From sound to synapse. Physiology of the mammalian ear. Oxford University Press, Oxford, pp 1–381Google Scholar
  25. Gonzalez-Soriano J, Mayayo-Vicente S, Martinez-Sainz P, Contreras-Rodriguez J, Rodriguez-Veiga E (1997) A quantitative study of ganglion cells in the goat retina. Anat Histol Embryol 26:39–44PubMedGoogle Scholar
  26. Greenwood DD (1962) Approximate calculation of the dimensions of traveling-wave envelopes in four species. J Acoust Soc Am 34:1364–1369Google Scholar
  27. Greenwood DD (1990) A cochlear frequency-position function for several species—29 years later. J Acoust Soc Am 87:2592–2605PubMedGoogle Scholar
  28. Gross EA, Swenberg JA, Fields S, Popp JA (1982) Comparative morphometry of the nasal cavity in rats and mice. J Anat 135:83–88PubMedGoogle Scholar
  29. Güntherschulze J (1979) Studien zur Kenntnis der Regio olfactoria von Wild- und Hausschwein (Sus scrofa scrofa L. 1768 und Sus scrofa f. domestica). Zool Anz 202:256–279Google Scholar
  30. Haque NM, Vijayan V (1993) Food habits of the fishing cat Felis viverrina in Keoladeo National Park, Bharatpur, Rajasthan. J Bombay Nat Hist Soc 90:498–500Google Scholar
  31. Heffner R, Heffner H (1980) Hearing in the elephant. Science 208:518–520PubMedGoogle Scholar
  32. Heffner RS, Heffner HE (1992) Visual factors in sound localization in mammals. J Comp Neurol 317:219–232PubMedGoogle Scholar
  33. Heffner RS, Heffner HE (2010) Explaining high-frequency hearing. Anat Rec 293:2080–2082Google Scholar
  34. Heffner H, Masterton B (1980) Hearing in Glires: domestic rabbit, cotton rat, feral house mouse, and kangaroo rat. J Acoust Soc Am 68:1584–1599Google Scholar
  35. Heffner RS, Koay G, Heffner HE (2001) Audiograms of five species of rodents: implications for the evolution of hearing and the perception of pitch. Hearing Res 157:138–152Google Scholar
  36. Hemilä S, Reuter T (2008) The physics and biology of olfaction and taste. In: Thewissen JGM, Nummela S (eds) Sensory evolution on the threshold: adaptations in secondarily aquatic vertebrates. University of California Press, Berkeley, pp 29–33Google Scholar
  37. Hemilä S, Nummela S, Reuter T (1995) What middle ear parameters tell about impedance matching and high frequency hearing. Hearing Res 85:31–44Google Scholar
  38. Hemilä S, Nummela S, Reuter T (2010) Anatomy and physics of the exceptional sensitivity of dolphin hearing (Odontoceti: Cetacea). J Comp Physiol A 196:165–179Google Scholar
  39. Henderson Z (1985) Distribution of ganglion cells in the retina of adult pigmented ferret. Brain Res 358:221–228PubMedGoogle Scholar
  40. Henson OW Jr (1961) Some morphological and functional aspects of certain structures of the middle ear in bats and insectivores. Univ Kansas Sci Bull 42:151–255Google Scholar
  41. Hirsch J, Curcio CA (1989) The spatial resolution capacity of human foveal retina. Vision Res 29:1095–1101PubMedGoogle Scholar
  42. Hodgkin AL (1964) The conduction of the nervous impulse. Liverpool University Press, Liverpool, pp 1–108Google Scholar
  43. Howland HC, Merola S, Basarab JR (2004) The allometry and scaling of the size of vertebrate eyes. Vision Res 44:2043–2065PubMedGoogle Scholar
  44. Hughes A (1975) A comparison of retinal ganglion cell topography in the plains and tree kangaroo. J Physiol 244:61P–63PPubMedGoogle Scholar
  45. Hughes A (1977) The topography of vision in mammals of contrasting life style: comparative optics and retinal organization. In: Crescitelli F (ed) Handbook of sensory physiology. The visual system in vertebrates, vol VII/5. Springer, Berlin, pp 613–756Google Scholar
  46. Kendall DG (1989) A survey of the statistical theory of shape. Stat Sci 4:87–120Google Scholar
  47. Ketten DR (2000) Cetacean ears. In: Au WWL, Popper AN, Fay RR (eds) Hearing by whales and dolphins. Springer, New York, pp 43–108Google Scholar
  48. Kiltie RA (2000) Scaling of visual acuity with body size in mammals and birds. Funct Ecol 14:226–234Google Scholar
  49. King AJ (1999) Sensory experience and the formation of a computational map of auditory space in the brain. BioEssays 21:900–911PubMedGoogle Scholar
  50. Kolb A (1971) Licht- und elektronenmikroskopische Untersuchungen der Nasenhöhle und des Riechepithels einiger Fledermausarten. Z Säugertierk 36:202–213Google Scholar
  51. Kolb A (1975) Lichtmikroskopische Untersuchungen am Riechepithel des Rehes (Capreolus capreolus). Anat Anz 137:417–428PubMedGoogle Scholar
  52. Lange S, Stalleicken J, Burda H (2004) Functional morphology of the ear in fossorial rodents, Microtus arvalis and Arvicola terrestris. J Morphol 262:770–779PubMedGoogle Scholar
  53. Laska M, Seibt A (2002) Olfactory sensitivity for aliphatic alcohols in squirrel monkeys and pigtail macaques. J Exp Biol 205:1633–1643PubMedGoogle Scholar
  54. Lehmann EL, Romano JP (2005) Testing statistical hypotheses, III edn. Springer, New York, pp 1–786Google Scholar
  55. Liow LH, Fortelius M, Bingham E, Lintulaakso K, Mannila H, Flynn L, Stenseth NC (2008) Higher origination and extinction rates in larger mammals. Proc Natl Acad Sci USA 105:6097–6102PubMedGoogle Scholar
  56. Liu L, Puolamäki K, Eronen JT, Ataabadi MM, Hernesniemi E, Fortelius M (2012) Dental functional traits of mammals resolve productivity in terrestrial ecosystems past and present. Proc R Soc B 279:2793–2799PubMedGoogle Scholar
  57. Louage DHG, van der Heijden M, Joris PX (2005) Enhanced temporal response properties of anteroventral cochlear nucleus neurons to broadband noise. J Neurosci 25:1560–1570PubMedGoogle Scholar
  58. Manoussaki D, Chadwick RS, Ketten DR, Arruda J, Dimitriadis EK, O′Malley JT (2008) The influence of cochlear shape on low-frequency hearing. Proc Natl Acad Sci USA 105:6162–6166PubMedGoogle Scholar
  59. Mass AM, Supin AY (1992) Peak density, size and regional distribution of ganglion cells in the retina of the fur seal Callorhinus ursinus. Brain Behav Evol 39:69–76PubMedGoogle Scholar
  60. Mass AM, Supin AY (2000) Ganglion cells density and retinal resolution in the sea otter, Enhydra lutris. Brain Behav Evol 55:111–119PubMedGoogle Scholar
  61. Mass AM, Supin AY (2003) Retinal topography of the harp seal Pagophilus groenlandicus. Brain Behav Evol 62:212–222PubMedGoogle Scholar
  62. Muchlinski MN (2010) A comparative analysis of vibrissa count and infraorbital foramen area in primates and other mammals. J Hum Evol 58:447–473PubMedGoogle Scholar
  63. Müller M, Wess F-P, Bruns V (1993) Cochlear place-frequency map in the marsupial Monodelphis domestica. Hearing Res 67:198–202Google Scholar
  64. Mulvaney BD, Heist HE (1970) Mapping of rabbit olfactory cells. J Anat 107:19–30PubMedGoogle Scholar
  65. Murphy WJ, Pringle TH, Crider TA, Springer MS, Miller W (2007) Using genomic data to unravel the root of the placental mammal phylogeny. Genome Res 17:413–421PubMedGoogle Scholar
  66. Musacchia G, Sams M, Nicol T, Kraus N (2006) Seeing speech affects acoustic information processing in the human brainstem. Exp Brain Res 168:1–10PubMedGoogle Scholar
  67. Niven JE, Laughlin SB (2008) Energy limitation as a selective pressure on the evolution of sensory systems. J Exp Biol 211:1792–1804PubMedGoogle Scholar
  68. Nowak RM (1999) Walker′s mammals of the world, vol 1–2, VI edn. The Johns Hopkins University Press, Baltimore, pp 1–2015Google Scholar
  69. Nummela S (1995) Scaling of the mammalian middle ear. Hearing Res 85:18–30Google Scholar
  70. Nummela S (1997) Scaling and modeling the mammalian middle ear. Comments Theor Biol 4:387–412Google Scholar
  71. Nummela S, Sánchez-Villagra MR (2006) Scaling of the marsupial middle ear and its functional significance. J Zool 270:256–267Google Scholar
  72. Nummela S, Thewissen JGM, Bajpai S, Hussain ST, Kumar K (2004) Eocene evolution of whale hearing. Nature 430:776–778PubMedGoogle Scholar
  73. Oelschläger HA (1989) Early development of the olfactory and terminalis systems in baleen whales. Brain Behav Evol 34:171–184PubMedGoogle Scholar
  74. Okawa H, Sampath AP, Laughlin SB, Fain GL (2008) ATP consumption by mammalian rod photoreceptors in darkness and in light. Curr Biol 18:1917–1921PubMedGoogle Scholar
  75. Peichl L (1992) Topography of ganglion cells in the dog and wolf retina. J Comp Neurol 324:603–620PubMedGoogle Scholar
  76. Peichl L (2005) Diversity of mammalian photoreceptor properties: adaptation to habitat and lifestyle? Anat Rec A 287A:1001–1012Google Scholar
  77. Pettigrew JD, Dreher B, Hopkins CS, McCall MJ, Brown M (1988) Peak density and distribution of ganglion cells in the retinae of microchiropteran bats: implications for visual acuity. Brain Behav Evol 32:39–56PubMedGoogle Scholar
  78. Pettigrew JD, Bhagwandin A, Haagensen M, Manger PR (2010) Visual acuity and heterogeneities of retinal ganglion cell densities and the tapetum lucidum of the African elephant (Loxodonta africana). Brain Behav Evol 75:251–261PubMedGoogle Scholar
  79. Pihlström H (2008) Comparative anatomy and physiology of chemical senses in aquatic mammals. In: Thewissen JGM, Nummela S (eds) Sensory evolution on the threshold: adaptations in secondarily aquatic vertebrates. University of California Press, Berkeley, pp 95–109Google Scholar
  80. Pihlström H, Fortelius M, Hemilä S, Forsman R, Reuter T (2005) Scaling of mammalian ethmoid bones can predict olfactory organ size and performance. Proc R Soc B 272:957–962PubMedGoogle Scholar
  81. Plassmann W, Brändle K (1992) A functional model of the auditory system in mammals and its evolutionary implications. In: Webster WB, Fay RR, Popper AN (eds) The evolutionary biology of hearing. Springer, New York, pp 637–653Google Scholar
  82. Pollak GD (1992) Adaptations of basic structures and mechanisms in the cochlea and central auditory pathway of the Mustache bat. In: Webster WB, Fay RR, Popper AN (eds) The evolutionary biology of hearing. Springer, New York, pp 751–778Google Scholar
  83. Polly PD, Eronen JT, Fred M, Dietl GP, Mosbrugger V, Scheidegger C, Frank DC, Damuth J, Stenseth NC, Fortelius M (2011) History matters: ecometrics and integrative climate change biology. Proc R Soc B 278:1131–1140PubMedGoogle Scholar
  84. Proops L, McComb K, Reby D (2009) Cross-modal individual recognition in domestic horses (Equus caballus). Proc Natl Acad Sci USA 106:947–951PubMedGoogle Scholar
  85. Pye A (1985–1986) Analysis of some cochlear components from surface preparations in bats. Myotis 23–24:51–55Google Scholar
  86. Radinsky LB (1968) Evolution of somatic sensory specialization in otter brains. J Comp Neurol 134:495–506PubMedGoogle Scholar
  87. Reiss JO, Eisthen HL (2008) Comparative anatomy and physiology of chemical senses in amphibians. In: Thewissen JGM, Nummela S (eds) Sensory evolution on the threshold: adaptations in secondarily aquatic vertebrates. University of California Press, Berkeley, pp 43–63Google Scholar
  88. Reuter T, Peichl L (2008) Structure and function of the retina in aquatic tetrapods. In: Thewissen JGM, Nummela S (eds) Sensory evolution on the threshold: adaptations in secondarily aquatic vertebrates. University of California Press, Berkeley, pp 149–172Google Scholar
  89. Ritland SM (1982) The allometry of the vertebrate eye. Dissertation, The University of ChicagoGoogle Scholar
  90. Rodieck RW (1998) The first steps in seeing. Sinauer Associates, Sunderland, pp 1–562Google Scholar
  91. Rosowski JJ (1992) Hearing in transitional mammals: predictions from the middle-ear anatomy and hearing capabilities. In: Webster WB, Fay RR, Popper AN (eds) The evolutionary biology of hearing. Springer, New York, pp 615–631Google Scholar
  92. Rosowski JJ, Graybeal A (1991) What did Morganucodon hear? Zool J Linn Soc 101:131–168Google Scholar
  93. Rouquier S, Blancher A, Giorgi D (2000) The olfactory receptor gene repertoire in primates and mouse: evidence for reduction of the functional fraction in primates. Proc Natl Acad Sci USA 97:2870–2874PubMedGoogle Scholar
  94. Rowe TB, Eiting TP, Macrini TE, Ketcham RA (2005) Organization of the olfactory and respiratory skeleton in the nose of the gray short-tailed opossum Monodelphis domestica. J Mammal Evol 12:303–336Google Scholar
  95. Sams M, Aulanko R, Hämäläinen M, Hari R, Lounasmaa O, Lu S-T, Simola J (1991) Seeing speech: visual information from lip movements modifies activity in the human auditory cortex. Neurosci Lett 127:141–145PubMedGoogle Scholar
  96. Sánchez-Villagra MR, Asher RJ (2002) Cranio-sensory adaptations in small faunivorous semiaquatic mammals, with special reference to olfaction and the trigeminal system. Mammalia 66:93–109Google Scholar
  97. Seyfarth RM, Cheney DL (2009) Seeing who we hear and hearing who we see. Proc Natl Acad Sci USA 106:669–670PubMedGoogle Scholar
  98. Sigmund L, Sedláček F (1985) Morphometry of the olfactory organ and olfactory thresholds of some fatty acids in Sorex araneus. Acta Zool Fenn 173:249–251Google Scholar
  99. Smith CUM (2000) Biology of sensory systems. Wiley, Chichester, pp 1–445Google Scholar
  100. Smith TD, Rossie JB, Bhatnagar KP (2007) Evolution of the nose and nasal skeleton in primates. Evol Anthropol 16:132–146Google Scholar
  101. Söllner B, Kraft R (1980) Anatomie und Histologie der Nasenhöhle der Europäischen Wasserspitzmaus, Neomys fodiens (Pennant 1771), und anderer mitteleuropäischer Soriciden. Spixiana 3:251–272Google Scholar
  102. Spoor F, Bajpai S, Hussain ST, Kumar K, Thewissen JGM (2002) Vestibular evidence for the evolution of aquatic behaviour in early cetaceans. Nature 417:163–166PubMedGoogle Scholar
  103. Steindorff K (1947) Deskriptive Anatomie des Auges der Wirbeltiere und des Menschen. Tabulae Biol 22:166–297PubMedGoogle Scholar
  104. Stevens M (2013) Sensory ecology, behaviour, and evolution. Oxford University Press, Oxford, pp 1–247Google Scholar
  105. Stone J (1965) A quantitative analysis of the distribution of ganglion cells in the cat’s retina. J Comp Neurol 124:337–352PubMedGoogle Scholar
  106. Stone J, Halasz P (1989) Topography of the retina in the elephant Loxodonta africana. Brain Behav Evol 34:84–95PubMedGoogle Scholar
  107. Supin AY, Popov VV, Mass AM (2001) The sensory physiology of aquatic mammals. Kluwer Academic Publishers, Boston, pp 1–332Google Scholar
  108. Suthers RA, Wallis NE (1970) Optics of the eyes of echolocation bats. Vis Res 10:1165–1173PubMedGoogle Scholar
  109. West CD (1985) The relationship of the spiral turns of the cochlea and the length of the basilar membrane to the range of audible frequencies in ground dwelling mammals. J Acoust Soc Am 77:1091–1101PubMedGoogle Scholar
  110. Wilson DM, Reeder DA (eds) (2005) Mammal species of the world: a taxonomic and geographical reference, III edn. Johns Hopkins University Press, Baltimore, pp 1–2142Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Sirpa Nummela
    • 1
  • Henry Pihlström
    • 1
  • Kai Puolamäki
    • 2
  • Mikael Fortelius
    • 3
  • Simo Hemilä
    • 1
  • Tom Reuter
    • 1
  1. 1.Department of BiosciencesUniversity of HelsinkiHelsinkiFinland
  2. 2.Department of Information and Computer ScienceAaltoFinland
  3. 3.Department of Geosciences and GeographyUniversity of HelsinkiHelsinkiFinland

Personalised recommendations