Complexity and a Coupled System: Flight, Echolocation and Evolution in Bats

  • J. M. V. Rayner

Summary

Flight places extreme pressures on mechanical and physiological systems capable of supplying energy for flight and structural strength to accommodate aerodynamic and inertial loads. Severe demands of echolocation are manifest mostly in neurology and behaviour. Echolocation with ultrasound is characteristic of microchiropteran bats, being used for orientation, prey detection and target ranging. Microbats are highly aerial animals relying almost entirely on flight for locating food; they represent an important model for studying the evolutionary interaction of echolocation and flight, two coupled adaptive domains.

This chapter reviews coupling between echolocation and flight in bats. The linked optimization of locomotory and sensory performance has been a major feature of the adaptation and radiation of bats.
  1. 1.

    Mechanical Linkage Between Echolocation and Flight. Flying bats omit echolocation calls during the upstroke when the pectoralis generates its peak force and the thorax is compressed. Microbats may not emit sound pulses while gliding.

     
  2. 2.

    Call Design, Flight Patterns and Community Structure. Bat communities are structured by the flight and echolocation in enabling a bat to move around its habitat and to find and catch prey. Species show a range of feeding patterns, which correlate with morphological adaptations favouring appropriate flight patterns and with echolocation call design.

     
  3. 3.

    Echolocation and Prey Capture. Bats hawking insects search for prey by echolocation. Prey location involves a decision on viability (catching the item must be mechanically possible and energetically profitable), and then the flight path must be controlled to intersect the prey. Sensory information, motor control and flapping flight force generation must be integrated, and echolocation and flight design must impose constraints on prédation.

     
  4. 4.

    Evolution of Bats, Flight and Echolocation. Adaptive paradigms should be studied within a phylogenetic framework. Bats are traditionally considered a monophyletic group within the Mammalia but brain, eye-brain pathways and echolocation characters link megabats with primates. Further evidence is provided by the wings, which show significant anatomical and osteological differences, and the fossil record, which in non-echolocating megabats is markedly more recent than microbats. Bats do not form a natural taxonomic group but are diphyle-tic, and the membranous wing supported by elongated digits is homoplasic; megabats are probably a sister group of primates. Differences in size and the absence of echolocation as a primitive character in megabats suggest possible differences in the evolution of flight in the two groups.

     

Keywords

Biomass Vortex Respiration Hunt Stein 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aldridge HDJN (1985) Manoeuvrability and ecology in British bats. Myotis 23–24:157–160Google Scholar
  2. Aldridge HDJN (1986) Manoeuvrability and ecological segregation in the little brown (Myotis lucifugus) and Yuma (M. yumanensis) bats (Chiroptera: Vespertilionidae). Can J Zool 64: 1878–1882CrossRefGoogle Scholar
  3. Aldridge HDJN, Rautenbach IL (1987) Morphology, echolocation and resource partitioning in insectivorous bats. J Anim Ecol 56:763–778CrossRefGoogle Scholar
  4. Altenbach JS, Hermanson J (1987) Bat flight muscle function and kinematics at the scapulo-humeral lock. In: Fenton MB, Racey PA, Rayner JMV (eds) Recent advances in the study of bats. Cambridge Univ Press, Cambridge, Mass, pp 100–118Google Scholar
  5. Anderson MA (1990) Feeding behaviour and echolocation in the brown-long-eared bat, Plecotus auritus. In: Hanak V, Horacek I, Gaisler J (eds) European bat research 1987. Proc 4th Eur Bat Res Symp, Praha 1987. Charles Univ Press, Praha (in press)Google Scholar
  6. Baagøe HJ (1987) The Scandinavian bat fauna: adaptive wing morphology and free flight in the field. In: Fenton MB, Racey PA, Rayner JMV (eds) Recent advances in the study of bats. Cambridge Univ Press, Cambridge, Mass, pp 57–74Google Scholar
  7. Beard K (1990) Gliding behaviour and palaeoecology of the alleged primate family Paromyidae (Mammalia, Dermoptera). Nature (London) 345:340–341CrossRefGoogle Scholar
  8. Brown PL, Brown TW, Grinnell AD (1983) Echolocation, development, and vocal communication in the lesser bulldog bat, Noctilio albiventris. Behav Ecol Sociobiol 13:287–298CrossRefGoogle Scholar
  9. Buchler ER (1980) The development of flight, foraging and echolocation in the little brown bat (Myotis lucifugus). Behav Ecol Sociobiol 6:211–218CrossRefGoogle Scholar
  10. Dial KP, Kaplan SR, Goslow GE, Jenkins FA (1988) A functional analysis of the primary upstroke and downstroke muscles in the domestic pigeon (Columba livid). J Exp Biol 134:1–16PubMedGoogle Scholar
  11. Fenton MB (1984) Echolocation: implications for ecology and evolution of bats. Q Rev Biol 59:33–53CrossRefGoogle Scholar
  12. Fenton MB (1985) Communication in the Chiroptera. Indiana Univ Press, BloomingtonGoogle Scholar
  13. Fiedler J (1979) Prey catching with and without echolocation in the Indian false vampire bat Megader-ma lyra. Behav Ecol Sociobiol 6:155–160CrossRefGoogle Scholar
  14. Findley JS (1976) The structure of bat communities. Am Nat 110:129–139CrossRefGoogle Scholar
  15. Findley JS, Black H (1983) Morphological and dietary structuring of a Zambian insectivorous bat community. Ecology 64:625–630CrossRefGoogle Scholar
  16. Goslow GE, Dial KP, Jenkins FA (1989) The avian shoulder: an experimental approach. Am Zool 29:287–301Google Scholar
  17. Goslow GE, Dial KP, Jenkins FA (1990) Bird flight: insights and complications. BioScience 40:108–115CrossRefGoogle Scholar
  18. Gould E (1988) Wing-clapping sounds of Eonycteris spelaea (Pteropodidae) in Malaysia. J Mammal 69:378–379CrossRefGoogle Scholar
  19. Griffin DR (1958) Listening in the dark. Yale Univ Press, New HavenGoogle Scholar
  20. Griffin DR, Webster FA, Michael CR (1960) The echolocation of flying insects by bats. Anim Behav 8:141–154CrossRefGoogle Scholar
  21. Habersetzer J (1986) Vergleichende flügelmorphologische Untersuchungen an einer Fledermausgesellschaft in Madurai. In: Nachtigall W (ed) Biona Report 5, Bat flight — Fledermausflug. Fischer, Stuttgart, pp 75–104Google Scholar
  22. Habersetzer J, Marimuthu G (1986) Ontogeny of sounds in the echolocating bat Hipposideros speoris. J Comp Physiol A 158:247–257CrossRefGoogle Scholar
  23. Habersetzer J, Storch G (1987) Klassifikation und funktionelle Flügelmorphologie paläogener Fledermäuse (Mammalia, Chiroptera). Cour Forsch Inst Senckenb 91:117–150Google Scholar
  24. Heblich K (1986) Flügelschlag und Lautaussendung bei fliegenden und landenden Fledermäusen. In: Nachtigall W (ed) Biona Report 5, Bat flight — Fledermausflug. Fischer, Stuttgart, pp 139–156Google Scholar
  25. Heller K-G, Heiversen O von (1989) Resource partitioning of sonar frequency bands in rhinolophid bats. Oecologia 80:178–186Google Scholar
  26. Herbert H (1986) Korrelation zwischen Flügelschlag und Ortungslautaussendung bei fliegenden und landenden Flughunden Rousettus aegyptiacus. In: Nachtigall W (ed) Biona Report 5, Bat flight — Fledermausflug. Fischer, Stuttgart, pp 157–168Google Scholar
  27. Hermanson JW, Altenbach JS (1981) Functional anatomy of the primary downstroke muscles in the pallid bat, Antrozous pallidus. J Mammal 62:795–800CrossRefGoogle Scholar
  28. Hermanson JW, Altenbach JS (1983) The functional anatomy of the shoulder of the pallid bat, Antrazous pallidus. J Mammal 64:62–75CrossRefGoogle Scholar
  29. Hermanson JW, Altenbach JS (1985) Functional anatomy of the shoulder and arm of the fruit-eating bat Artibeus jamaicensis. J Zool London Ser A 205:157–177CrossRefGoogle Scholar
  30. Jenkins FA, Dial KP, Goslow GE (1988) A cineradiographic analysis of bird flight: the wishbone in starlings is a spring. Science 241:1495–1498PubMedCrossRefGoogle Scholar
  31. Jepsen GL (1966) Early Eocene bat from Wyoming. Science 154:1333–1339PubMedCrossRefGoogle Scholar
  32. Jepsen GL (1970) Bat origins and evolution. In: Wimsatt WA (ed) Biology of bats, vol 1. Academic Press, New York London, pp 1–64Google Scholar
  33. Jones G, Rayner JMV (1988) Flight performance, foraging tactics and echolocation in free-living Daubenton’s bats Myotis daubentoni (Chiroptera: Vespertilionidae). J Zool, London 215:113–132CrossRefGoogle Scholar
  34. Jones G, Rayner JMV (1989) Echolocation and foraging behavior of wild horseshoe bats Rhinolophus ferrumequinum and R. hipposideros (Chiroptera, Rhinolophidae). Behav Ecol Sociobiol 25:183–191CrossRefGoogle Scholar
  35. Kalko EKV, Schnitzler H-U (1989) The echolocation and hunting behavior of Daubenton’s bat, Myotis daubentoni. Behav Ecol Sociobiol 24:225–238CrossRefGoogle Scholar
  36. Konstantinov AI, Makarov AK (1987) [Formation of echolocation in ontogenesis of the bat Rhinolophus ferrumequinum.] Zh Evol Biokhim Fiziol 23:98–109Google Scholar
  37. Kovtun MF (1985) The evolutionary morphology of locomotion organs system in bats (Mammalia: Chiroptera). In: Mlikovsky J, Novak VJA (eds) Evolution and morphology. Acadecmica, Praha, pp 589–596Google Scholar
  38. Leche W (1886) Über die Säugethiergattung Goeleopithecus. Kgl Svensk Vet-Akad Handl 21(11):1–92Google Scholar
  39. McKenzie NL, Rolfe JK (1986) Structure of bat guilds in the Kimberley mangroves, Australia. J Anim Ecol 55:401–420CrossRefGoogle Scholar
  40. Miller GS (1907) The families and genera of bats. Bull US Nat Mus 57CrossRefGoogle Scholar
  41. Neuweiler G (1989) Foraging ecology and audition in echolocating bats. TREE 4:160–166PubMedGoogle Scholar
  42. Neuweiler G, Metzner W, Heilmann U, Rübsamen R, Eckrich M, Costa HH (1987) Foraging behaviour and echolocation in the rufous horseshoe bat (Rhinolophus rouxi) of Sri Lanka. Behav Ecol Sociobiol 20:53–67CrossRefGoogle Scholar
  43. Norberg UM (1986) Evolutionary convergence in foraging niche and flight morphology in insectivorous aerial-hawking birds and bats. Ornis Scand 17:253–260CrossRefGoogle Scholar
  44. Norberg UM (1990 a) Vertebrate flight: mechanics, physiology, morphology, ecology and evolution. Springer, Berlin Heidelberg New York TokyoGoogle Scholar
  45. Norberg UM (1990 b) Ecological determinants of bat wing shape and echolocation call structure with implications for some fossil bats. In: Hanak V, Horacek I, Gaisler J (eds) European bat research 1987. Proc 4th Eur Bat Res Symp, Praha 1987. Charles Univ Press, Praha (in press)Google Scholar
  46. Norberg UM, Rayner JMV (1987) Ecological morphology and flight in bats (Mammalia, Chiroptera): wing adaptations, flight performance, foraging strategies and echolocation. Philos Trans R Soc London Ser B 316:335–427CrossRefGoogle Scholar
  47. Novacek MJ (1985) Evidence for echolocation in the oldest known bats. Nature (London) 315:140–141CrossRefGoogle Scholar
  48. O’Neill MGO, Taylor RJ (1986) Observations on the flight patterns and foraging behaviour of Tasmanian bats. Aust Wildl Res 13:427–432CrossRefGoogle Scholar
  49. Padian K (1982) Macroevolution and the origin of major adaptations: vertebrate flight as a paradigm for the analysis of patterns. Proc 3rd N Am Paleontol Convention, vol 2, pp 381–392Google Scholar
  50. Padian K (1987) A comparative phylogenetic and functional approach to the origin of vertebrate flight. In: Fenton MB, Racey PA, Rayner JMV (eds) Recent advances in the study of bats. CambridgeUniv Press, Cambridge, Mass, pp 3–19Google Scholar
  51. Pettigrew JD (1986) Flying primates? Megabats have the advanced pathway from eye to midbrain. Science 231:1304–1306PubMedCrossRefGoogle Scholar
  52. Pettigrew JD, Jamieson BGM, Robson SK, Hall LS, McNally KI, Cooper HM (1989) Phylogenetic relations between microbats, megabats and primates (Mammalia: Chiroptera and Primates). Philos Trans R Soc London Ser B 325:489–559CrossRefGoogle Scholar
  53. Pollak GD, Casseday JH (1989) The neural basis of echolocation in bats. Springer, Berlin Heidelberg New York TokyoCrossRefGoogle Scholar
  54. Rayner JMV (1986) Vertebrate flapping flight mechanics and aerodynamics, and the evolution of flight in bats. In: Nachtigall W (ed) Biona Report 5, Bat flight — Fledermausflug. Fischer, Stuttgart, pp 27–74Google Scholar
  55. Rayner JMV (1987) The mechanics of flapping flight in bats. In: Fenton MB, Racey PA, Rayner JMV (eds) Recent advances in the study of bats. Cambridge Univ Press, Cambridge, Mass, pp 23–42Google Scholar
  56. Rayner JMV (1988 a) Form and function in avian flight. Curr Ornithol 5:1–77Google Scholar
  57. Rayner JMV (1988b) The evolution of vertebrate flight. Biol J Linn Soc 34:269–287CrossRefGoogle Scholar
  58. Rayner JMV (1989 a) Mechanics and physiology of flight in fossil and recent vertebrates. Trans R Soc Edinburgh Earth Sci 80:311–320CrossRefGoogle Scholar
  59. Rayner JMV (1989 b) Vertebrate flight and the origins of flying vertebrates. In: Allen KC, Briggs DEG (eds) Palaeoecology and palaeoenvironments. Belhaven, London, pp 188–217Google Scholar
  60. Richter G, Storch G (1980) Beiträge zur Ernährungsbiologie eozäner Fledermäuse aus der “Grube Messer’. Nat Mus 110:353–367Google Scholar
  61. Rose KD, Simons EL (1977) Dental function in the Plagiomenidae: origin and relationships of the mammalian order Dermoptera. Contrib Mus Paleontol Univ Mich 24:221–236Google Scholar
  62. Rübsamen R (1987) Ontogenesis of the echolocation system in the rufous horseshoe bat, Rhinolophus rouxi (Audition and vocalization in early postnatal development). J Comp Physiol A 161:899–913PubMedCrossRefGoogle Scholar
  63. Schnitzler H-U (1971) Fledermäuse im Windkanal. Z Vergl Physiol 73:209–221CrossRefGoogle Scholar
  64. Schnitzler H-U, Henson OW (1980) Performance of airborne animal sonar systems, I Microchiroptera. In: Busnel R-G, Fish JF (eds) Animal sonar systems. Plenum New York, pp 109–181Google Scholar
  65. Schnitzler H-U, Hackbarth H, Heilmann U, Herbert H (1985) Echolocation behavior of rufous horseshoe bats hunting for insects in the flycatcher-style. J Comp Physiol A 157:39–46CrossRefGoogle Scholar
  66. Schnitzler H-U, Kalko E, Miller L, Surlykke A (1987) The echolocation and hunting behavior of the bat, Pipistrellus kuhli. J Comp Physiol A 161:267–274PubMedCrossRefGoogle Scholar
  67. Scholey KD (1986) The evolution of flight in bats. In: Nachtigall W (ed) Biona Report 5, Bat flight — Fledermausflug. Fischer, Stuttgart, pp 1–12Google Scholar
  68. Simmons JA (1987) Acoustic images of target range in the sonar of bats. Naval Res Rev 39:11–26Google Scholar
  69. Simmons JA, Kick SA (1983) Interception of flying insects by bats. In: Huber F, Markl D (eds) Neuroethology and behavioural physiology. Springer, Berlin Heidelberg New York Tokyo, pp 267–279CrossRefGoogle Scholar
  70. Simmons JA, Stein RA (1980) Acoustic imaging in bat sonar: echolocation signals and the evolution of echolocation. J Comp Physiol 135 A:61–84CrossRefGoogle Scholar
  71. Simmons JA, Fenton MB, O’Farrell MJ (1979) Echolocation and pursuit of prey by bats. Science 203:16–20PubMedCrossRefGoogle Scholar
  72. Smith JD (1977) Comments on flight and the evolution of bats. In: Hecht MK, Goody PC, Hecht BM (eds) Major problems in vertebrate evolution. Plenum, New York, pp 427–437Google Scholar
  73. Smith JD (1980) Chiropteran phylogenetics: introduction. In: Wilson DE, Gardner AL (eds) Proc 5th Int Bat Res Conf. Texas Tech Press, Lubbock, pp 233–244Google Scholar
  74. Speakman JR, Anderson ME, Racey PA (1989) The energy cast of echolocation in pipistrelle bats (Pipistrellus pipistrellus). J Comp Physiol A 165:679–685CrossRefGoogle Scholar
  75. Thomas ALR, Jones G, Rayner JMV, Hughes PM (1990) Intermittent gliding flight in pipistrelle bats (Pipistrellus pipistrellus) (Chiroptera: Vespertilionidae). J Exp Biol 149:407–416Google Scholar
  76. Van Valen L (1979) The evolution of bats. Evol Theor 4:103–121Google Scholar
  77. Webster F, Griffin D (1962) The role of the flight membrane in insect capture by bats. Anim Behav 10:322–340CrossRefGoogle Scholar
  78. Weid R, Helversen O von (1987) Ortungsrufe europäischer Fledermäuse beim Jagdflug im Freiland. Myotis 25:5–27Google Scholar
  79. Wible JR, Novacek MJ (1988) Cranial evidence for the monophyletic origin of bats. Am Mus Nov 2911Google Scholar
  80. Winge H (1941) The interrelationships of the mammalian genera, vol 1: Monotremata, Marsupialia, Insectivora, Chiroptera, Edentata. Reitzles, CopenhagenGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 1991

Authors and Affiliations

  • J. M. V. Rayner
    • 1
  1. 1.Department of ZoologyUniversity of BristolBristolUK

Personalised recommendations