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Behavioral Ecology and Sociobiology

, Volume 61, Issue 9, pp 1337–1348 | Cite as

Ecological niche and phylogeny: the highly complex echolocation behavior of the trawling long-legged bat, Macrophyllum macrophyllum

  • Moritz Weinbeer
  • Elisabeth K. V. KalkoEmail author
Original Paper

Abstract

Bats produce echolocation signals that reflect the sensory tasks they perform. In open air or over water, bats encounter few or no background echoes (clutter). Echolocation of such bats is the primary cue for prey perception and varies with the stage of approach to prey, typically comprising search, approach, and terminal group calls. In contrast, bats that glean stationary food from rough surfaces emit more uniform calls without a distinct terminal group. They use echolocation primarily for orientation in space and mostly need additional sensory cues for finding food because clutter echoes overlap strongly with food echoes. Macrophyllum macrophyllum is the only Neotropical leaf-nosed bat (Phyllostomidae) that hunts in clutter-poor habitat over water. As such, we hypothesized that, unlike all other members of its family, but similar to other trawling and aerial insectivorous bats, M. macrophyllum can hunt successfully by using only echolocation for prey perception. In controlled behavioral experiments on Barro Colorado Island, Panamá, we confirmed that echolocation alone is sufficient for finding prey in M. macrophyllum. Furthermore, we showed that pattern and structure of echolocation signals in M. macrophyllum are more similar to aerial and other trawling insectivorous bats than to close phylogenetic relatives. Particularly unique among phyllostomid bats, we found distinct search, approach, and terminal group calls in foraging M. macrophyllum. Call structure, however, consisting of short, multiharmonic, and steep frequency-modulated signals, closely resembled those of other phyllostomid bats. Thus, echolocation behavior in M. macrophyllum is shaped by ecological niche as well as by phylogeny.

Keywords

Barro Colorado Island Foraging behavior Phyllostomidae Sensory ecology Trawling 

Notes

Acknowledgements

We thank H.-U. Schnitzler for very valuable discussions, R. Page for highly beneficial comments on an earlier version of this manuscript, three anonymous reviewers for excellent advice, and the Smithsonian Tropical Research Institute (Panamá) for logistical assistance and excellent working conditions. Research was supported by a PhD stipend of the German Academic Exchange Study to Weinbeer and by a grant of the Deutsche Forschungsgemeinschaft (DFG KA-1241/5-1) to Kalko. The behavioral experiments complied with the current laws of Panamá.

References

  1. Altringham JD, Fenton MB (2003) Sensory ecology and communication in the Chiroptera. Bat Ecology 90–127Google Scholar
  2. Arita HT, Fenton MB (1997) Flight and echolocation in the ecology and evolution of bats. Trends Ecol Evol 12:53–58CrossRefGoogle Scholar
  3. Arlettaz R, Jones G, Racey PA (2001) Effect of acoustic clutter on prey detection by bats. Nature 414:742–745PubMedCrossRefGoogle Scholar
  4. Barclay RMR, Fenton MB, Tuttle MD, Ryan MJ (1981) Echolocation calls produced by Trachops cirrhosus (Chiroptera: Phyllostomidae) while hunting for frogs. Can J Zool 59:750–753Google Scholar
  5. Belwood JJ, Morris GK (1987) Bat predation and its influence on the calling behavior in Neotropical katydids. Science 238:64–67CrossRefPubMedGoogle Scholar
  6. Bonaccorso FJ (1979) Foraging and reproductive ecology in a Panamanian bat community. Bull Fla State Mus Biol Sci 24:359–408Google Scholar
  7. Boonman AM, Jones G (2002) Intensity control during target approach in echolocating bats; stereotypical sensory-motor behaviour in Daubenton’s bats, Myotis daubentonii. J Exp Biol 205:2865–2874PubMedGoogle Scholar
  8. Boonman A, Boonman M, Bretschneider F, van de Grind WA (1998) Prey detection in trawling insectivorous bats: duckweed affects hunting behaviour in Daubenton’s bat, Myotis daubentonii. Behav Ecol Sociobiol 44:99–107CrossRefGoogle Scholar
  9. Britton ARC, Jones G, Rayner JMV, Boonman AM, Verboom B (1997) Flight performance, echolocation and foraging behaviour in pond bats, Myotis dasycneme (Chiroptera: Vespertilionidae). J Zool 241:503–522Google Scholar
  10. Dusenbery DB (1992) Sensory ecology: how organisms acquire and respond to information. Freeman, New YorkGoogle Scholar
  11. Fenton MB (1990) The foraging behaviour and ecology of animal-eating bats. Can J Zool 68:411–422Google Scholar
  12. Fenton MB (1995) Natural history and biosonar signals. In: Popper AN, Fay RR (eds) Hearing by bats. Springer handbook of auditory research. Springer, New York, pp 37–86Google Scholar
  13. Fenton MB, Bell GP (1979) Echolocation and feeding behaviour in four species of Myotis (Chiroptera). Can J Zool 57:1271–1277Google Scholar
  14. Fenton MB, Rydell J, Vonhof MJ, Eklöf J, Lancaster WC (1999) Constant-frequency and frequency-modulated components in the echolocation calls of three species of small bats (Emballonuridae, Thyropteridae, and Vespertilionidae). Can J Zool 77:1891–1900CrossRefGoogle Scholar
  15. Giannini NP, Kalko EKV (2004) Trophic structure in a large assemblage of phyllostomid bats in Panama. Oikos 105:209–220CrossRefGoogle Scholar
  16. Griffin DR (1958) Listening in the dark. Yale University Press, New HavenGoogle Scholar
  17. Griffin DR, Webster FA, Michael CR (1960) The echolocation of flying insects by bats. Anim Behav 3:141–154CrossRefGoogle Scholar
  18. Harrison DL (1975) Macrophyllum macrophyllum. Mammalian Species 62:1–3CrossRefGoogle Scholar
  19. Holderied MV, von Helversen O (2003) Echolocation range and wingbeat period match in aerial-hawking bats. Proc R Soc Lond B 270:2293–2299CrossRefGoogle Scholar
  20. Hurlbert SH (1984) Pseudoreplication and the design of ecological field experiments. Ecol Monogr 54:187–211CrossRefGoogle Scholar
  21. Jones G, Rayner JMV (1988) Flight performance, foraging tactics and echolocation in free-living Daubenton’s bats Myotis daubentoni (Chiroptera: Vespertilionidae). J Zool 215:113–132CrossRefGoogle Scholar
  22. Jones G, Rayner JMV (1991) Flight performance, foraging tactics and echolocation in the trawling insectivorous bat Myotis adversus (Chiroptera: Vespertilionidae). J Zool 225:393–412CrossRefGoogle Scholar
  23. Jones KE, Purvis A, MacLarnon A, Bininda-Emonds ORP, Simmons NB (2002) A phylogenetic supertree of the bats (Mammalia: Chiroptera). Biol Rev 77:223–259PubMedCrossRefGoogle Scholar
  24. Kalko EKV (1995a) Echolocation signal design, foraging habitats and guild structure in six neotropical sheath-tailed bats (Emballonuridae). Symp Zool Soc Lond 67:259–273Google Scholar
  25. Kalko EKV (1995b) Insect pursuit, prey capture and echolocation in pipistrelle bats (Microchiroptera). Anim Behav 50:861–880CrossRefGoogle Scholar
  26. Kalko EKV (2004) Neotropical leaf-nosed bats (Phyllostomidae): “Whispering” bats or candidates for acoustic surveys? In: Brigham M, Jones G, Kalko EKV (eds) Proceedings of a workshop on identification and acoustic monitoring of bats. Bat Conservation International, Austin, TX, pp 63–69Google Scholar
  27. Kalko EKV, Condon MA (1998) Echolocation, olfaction and fruit display: How bats find fruit of flagellichorous cucurbits. Funct Ecol 12:364–372CrossRefGoogle Scholar
  28. Kalko EKV, Schnitzler H-U (1989) The echolocation and hunting behavior of Daubenton’s bat, Myotis daubentoni. Behav Ecol Sociobiol 24:225–238CrossRefGoogle Scholar
  29. Kalko EKV, Schnitzler H-U (1993) Plasticity in echolocation signals of European pipistrelle bats in search flight: implications for habitat use and prey detection. Behav Ecol Sociobiol 33:415–428CrossRefGoogle Scholar
  30. Kalko EKV, Schnitzler H-U, Kaipf I, Grinnell AD (1998) Echolocation and foraging behavior of the lesser bulldog bat, Noctilio albiventris: preadaptations for piscivory. Behav Ecol Sociobiol 42:305–319CrossRefGoogle Scholar
  31. Korine C, Kalko EKV (2005) Fruit detection and discrimination by small fruit-eating bats (Phyllostomidae): echolocation call design and olfaction. Behav Ecol Sociobiol 59:12–23CrossRefGoogle Scholar
  32. Meyer CFJ, Weinbeer M, Kalko EKV (2005) Home-range size and spacing patterns of Macrophyllum macrophyllum (Phyllostomidae) foraging over water. J Mammal 86:587–598CrossRefGoogle Scholar
  33. Neuweiler G (1990) Auditory adaptations for prey capture in echolocating bats. Physiol Rev 70:615–641PubMedGoogle Scholar
  34. Roverud RC, Nitsche V, Neuweiler G (1991) Discrimination of wingbeat motion by bats, correlated with echolocation sound pattern. J Comp Physiol A 168:259–263PubMedCrossRefGoogle Scholar
  35. Rydell J, Miller LA, Jensen ME (1999) Echolocation constraints of Daubenton’s bat foraging over water. Funct Ecol 13:247–255CrossRefGoogle Scholar
  36. Schnitzler H-U, Kalko EKV (1998) How echolocating bats search and find food. In: Kunz TH, Racey PA (eds) Bat biology and conservation. Smithsonian Institution, Washington, DC, pp 183–196Google Scholar
  37. Schnitzler H-U, Kalko EKV (2001) Echolocation by insect-eating bats. Bioscience 51:557–569CrossRefGoogle Scholar
  38. Schnitzler H-U, Kalko EKV, Miller M, Surlykke A (1987) The echolocation and hunting behavior of the bat, Pipistrellus kuhli. J Comp Physiol A 161:267–274PubMedCrossRefGoogle Scholar
  39. Schnitzler H-U, Kalko EKV, Kaipf I, Grinnell AD (1994) Fishing and echolocation behavior of the greater bulldog bat, Noctilio leporinus, in the field. Behav Ecol Sociobiol 35:327–345CrossRefGoogle Scholar
  40. Schnitzler H-U, Moss CF, Denzinger A (2003a) From spatial orientation to food acquisition in echolocating bats. Trends Ecol Evol 18:386–394CrossRefGoogle Scholar
  41. Schnitzler H-U, Kalko EKV, Denzinger A (2003b) The evolution of echolocation and foraging behavior in bats. In: Thomas JA, Moss C, Vater M (eds) Echolocation in bats and dolphins. University of Chicago Press, Chicago, pp 331–339Google Scholar
  42. Siemers BM, Schnitzler H-U (2000) Natterer’s bat ( Myotis nattereri Kuhl, 1818) hawks for prey close to vegetation using echolocation signals of very broad bandwidth. Behav Ecol Sociobiol 47:400–412CrossRefGoogle Scholar
  43. Siemers BM, Schnitzler H-U (2004) Echolocation signals reflect niche differentiation in five sympatric congeneric bat species. Nature 429:657–661PubMedCrossRefGoogle Scholar
  44. Siemers BM, Stilz P, Schnitzler H-U (2001a) The acoustic advantage of hunting at low heights above water: behavioural experiments on the European ‘trawling’ bats Myotis capaccinii, M. dasycneme and M. daubentonii. J Exp Biol 204:3843–3854PubMedGoogle Scholar
  45. Siemers BM, Kalko EKV, Schnitzler H-U (2001b) Echolocation behavior and signal plasticity in the Neotropical bat Myotis nigricans (Schinz, 1821) (Vespertilionidae): A convergent case with European species of Pipistrellus? Behav Ecol Sociobiol 50:317–328CrossRefGoogle Scholar
  46. Siemers BM, Baur E, Schnitzler H-U (2005) Acoustic mirror effect increases prey detection distance in trawling bats. Naturwissenschaften 92:272–276PubMedCrossRefGoogle Scholar
  47. Simmons JA, Stein RA (1980) Acoustic imaging in bat sonar: echolocation signals and the evolution of echolocation. J Comp Physiol A 135:61–84CrossRefGoogle Scholar
  48. Surlykke A, Moss CF (2000) Echolocation behavior of big brown bats, Eptesicus fuscus, in the field and the laboratory. J Acoust Soc Am 108:2419–2429PubMedCrossRefGoogle Scholar
  49. Suthers RA (1967) Comparative echolocation by fishing bats. J Mammal 48:79–87PubMedCrossRefGoogle Scholar
  50. Teeling EC, Springer MS, Madsen O, Bates P, O’Brien SJ, Murphy WJ (2005) A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307:580–584PubMedCrossRefGoogle Scholar
  51. Thies W, Kalko EKV, Schnitzler H-U (1998) The roles of echolocation and olfaction in two neotropical fruit-eating bats, Carollia perspicillata and C. castanea, feeding on Piper. Behav Ecol Sociobiol 42:397–409CrossRefGoogle Scholar
  52. Wiegrebe L, Schmidt S (1996) Temporal integration in the echolocating bat, Megaderma lyra. Hear Res 102:35–42PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  1. 1.Department of Experimental EcologyUniversity of UlmUlmGermany
  2. 2.Smithsonian Tropical Research InstituteBalboaPanamá

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