Adaptations in the call emission pattern of frugivorous bats when orienting under challenging conditions

Abstract

Echolocating bats emit biosonar calls and use echoes arising from call reflections, for orientation. They often pattern their calls into groups which increases the rate of sensory feedback. Insectivorous bats emit call groups at a higher rate when orienting in cluttered compared to uncluttered environments. Frugivorous bats increase the rate of call group emission when they echolocate in noisy environments. In frugivorous bats, it remains unclear if call group emission represents an exclusive adaptation to avoid acoustic interference by signals of conspecifics or if it represents an adaptation that allows to orient under demanding environmental conditions. Here, we compared the emission pattern of the frugivorous bat Carolliaperspicillata when the bats were flying in narrow versus wide or cluttered versus non-cluttered corridors. The bats emitted larger call groups and they increased the call rate within call groups when navigating in narrow or cluttered environments. These adaptations resemble the ones shown when the bats navigate in noisy environments. Thus, call group emission represents an adaptive behavior when the bats orient in complex environments.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Accomando AW, Vargas-Irwin CE, Simmons JA (2018) Spike train similarity space (SSIMS) method detects effects of obstacle proximity and experience on temporal patterning of bat biosonar. Front Behav Neurosci. https://doi.org/10.3389/fnbeh.2018.00013

    Article  PubMed  PubMed Central  Google Scholar 

  2. Amichai E, Blumrosen G, Yovel Y (2015) Calling louder and longer: how bats use biosonar under severe acoustic interference from other bats. Proc R Soc B-Biol Sci. https://doi.org/10.1098/rspb.2015.2064

    Article  Google Scholar 

  3. Bartenstein SK, Gerstenberg N, Vanderelst D, Peremans H, Firzlaff U (2014) Echo-acoustic flow dynamically modifies the cortical map of target range in bats. Nat Commun 5:4668. https://doi.org/10.1038/ncomms5668

    Article  CAS  PubMed  Google Scholar 

  4. Beetz MJ, Hechavarría JC, Kössl M (2016) Cortical neurons of bats respond best to echoes from nearest targets when listening to natural biosonar multi-echo streams. Sci Rep UK. https://doi.org/10.1038/srep35991

    Article  Google Scholar 

  5. Beetz MJ, Hechavarría JC, Kössl M (2016) Temporal tuning in the bat auditory cortex is sharper when studied with natural echolocation sequences. Sci Rep UK. https://doi.org/10.1038/srep29102

    Article  Google Scholar 

  6. Beetz MJ, Kordes S, Garcia-Rosales F, Kössl M, Hechavarría JC (2017) Processing of natural echolocation sequences in the inferior colliculus of Seba's fruit eating bat Carollia perspicillata. Eneuro. https://doi.org/10.1523/ENEURO.0314-17.2017

    Article  PubMed  PubMed Central  Google Scholar 

  7. Beetz MJ, Garcia-Rosales F, Kössl M, Hechavarría JC (2018) Robustness of cortical and subcortical processing in the presence of natural masking sounds. Sci Rep UK. https://doi.org/10.1038/s41598-018-25241-x

    Article  Google Scholar 

  8. Bentivoglio AR, Bressman SB, Cassetta E, Carretta D, Tonali P, Albanese A (1997) Analysis of blink rate patterns in normal subjects. Movement Disord 12(6):1028–1034. https://doi.org/10.1002/mds.870120629

    Article  CAS  PubMed  Google Scholar 

  9. Brinklov S, Kalko EKV, Surlykke A (2009) Intense echolocation calls from two 'whispering' bats, Artibeus jamaicensis and Macrophyllum macrophyllum (Phyllostomidae). J Exp Biol 212(1):11–20. https://doi.org/10.1242/jeb.023226

    Article  PubMed  Google Scholar 

  10. Brinklov S, Jakobsen L, Ratcliffe JM, Kalko EKV, Surlykke A (2011) Echolocation call intensity and directionality in flying short-tailed fruit bats, Carollia perspicillata (Phyllostomidae). J Acoust Soc Am 129(1):427–435. https://doi.org/10.1121/1.3519396

    Article  PubMed  Google Scholar 

  11. Falk B, Jakobsen L, Surlykke A, Moss CF (2014) Bats coordinate sonar and flight behavior as they forage in open and cluttered environments. J Exp Biol 217(24):4356–4364. https://doi.org/10.1242/jeb.114132

    Article  PubMed  PubMed Central  Google Scholar 

  12. Finneran JJ (2013) Dolphin “packet” use during long-range echolocation tasks. J Acoust Soc Am 133(3):1796–1810. https://doi.org/10.1121/1.4788997

    Article  PubMed  Google Scholar 

  13. Galambos R, Griffin DR (1942) Obstacle avoidance by flying bats—the cries of bats. J Exp Zool 89(3):475–490. https://doi.org/10.1002/jez.1400890308

    Article  Google Scholar 

  14. Geva-Sagiv M, Las L, Yovel Y, Ulanovsky N (2015) Spatial cognition in bats and rats: from sensory acquisition to multiscale maps and navigation. Nat Rev Neurosci 16(2):94–108. https://doi.org/10.1038/nrn3888

    Article  CAS  PubMed  Google Scholar 

  15. Gregoriou GG, Gotts SJ, Zhou HH, Desimone R (2009) High-frequency, long-range coupling between prefrontal and visual cortex during attention. Science 324(5931):1207–1210. https://doi.org/10.1126/science.1171402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Grinnell AD, Griffin DR (1958) The sensitivity of echolocation in bats. Biol Bull 114(1):10–22. https://doi.org/10.2307/1538961

    Article  Google Scholar 

  17. Gunduz A, Brunner P, Daitch A, Leuthardt EC, Ritaccio AL, Pesaran B, Schalk G (2011) Neural correlates of visual-spatial attention in electrocorticographic signals in humans. Front Hum Neurosci 5:89. https://doi.org/10.3389/fnhum.2011.00089

    Article  PubMed  PubMed Central  Google Scholar 

  18. Hechavarría JC, Macías S, Vater M, Voss C, Mora EC, Kössl M (2013) Blurry topography for precise target-distance computations in the auditory cortex of echolocating bats. Nat Commun. https://doi.org/10.1038/ncomms3587

    Article  PubMed  Google Scholar 

  19. Hiryu S, Bates ME, Simmons JA, Riquimaroux H (2010) FM echolocating bats shift frequencies to avoid broadcast-echo ambiguity in clutter. Proc Natl Acad Sci USA 107(15):7048–7053. https://doi.org/10.1073/pnas.1000429107

    Article  PubMed  Google Scholar 

  20. Hofmann V, Sanguinetti-Scheck JI, Kunzel S, Geurten B, Gomez-Sena L, Engelmann J (2013) Sensory flow shaped by active sensing: sensorimotor strategies in electric fish. J Exp Biol 216(13):2487–2500. https://doi.org/10.1242/jeb.082420

    Article  PubMed  Google Scholar 

  21. Ivanov MP (2004) Dolphin's echolocation signals in a complicated acoustic environment. Acoust Phys 50(4):469–479. https://doi.org/10.1134/1.1776226

  22. Kepecs A, Uchida N, Mainen ZF (2007) Rapid and precise control of sniffing during olfactory discrimination in rats. J Neurophysiol 98(1):205–213. https://doi.org/10.1152/jn.00071.2007

    Article  PubMed  Google Scholar 

  23. Kössl M, Hechavarría JC, Voss C, Macías S, Mora EC, Vater M (2014) Neural maps for target range in the auditory cortex of echolocating bats. Curr Opin Neurobiol 24:68–75. https://doi.org/10.1016/j.conb.2013.08.016

    Article  CAS  PubMed  Google Scholar 

  24. Kothari NB, Wohlgemuth MJ, Hulgard K, Surlykke A, Moss CF (2014) Timing matters: sonar call groups facilitate target localization in bats. Front Physiol. https://doi.org/10.3389/fphys.2014.00168

    Article  PubMed  PubMed Central  Google Scholar 

  25. Kothari NB, Wohlgemuth MJ, Moss CF (2018) Adaptive sonar call timing supports target tracking in echolocating bats. J Exp Biol. https://doi.org/10.1242/jeb.176537

    Article  PubMed  Google Scholar 

  26. Kothari NB, Wohlgemuth MJ, Moss CF (2018) Dynamic representation of 3D auditory space in the midbrain of the free-flying echolocating bat. Elife. https://doi.org/10.7554/eLife.29053

    Article  PubMed  PubMed Central  Google Scholar 

  27. Ladegaard M, Mulsow J, Houser DS, Jensen FH, Johnson M, Madsen PT, Finneran JJ (2018) Dolphin echolocation behaviour during active long-range target approaches. J Exp Biol. https://doi.org/10.1242/jeb.189217

    Article  Google Scholar 

  28. Luo JH, Goerlitz HR, Brumm H, Wiegrebe L (2015) Linking the sender to the receiver: vocal adjustments by bats to maintain signal detection in noise. Sci Rep UK. https://doi.org/10.1038/srep18556

    Article  Google Scholar 

  29. Madsen PT, Kerr I, Payne R (2004) Echolocation clicks of two free-ranging, oceanic delphinids with different food preferences: false killer whales Pseudorca crassidens and Risso's dolphins Grampus griseus. J Exp Biol 207(11):1811–1823. https://doi.org/10.1242/jeb.00966

    Article  CAS  PubMed  Google Scholar 

  30. Martin LM, Garcia-Rosales F, Beetz MJ, Hechavarría JC (2017) Processing of temporally patterned sounds in the auditory cortex of Seba's short-tailed bat Carollia perspicillata. Eur J Neurosci 46(8):2365–2379. https://doi.org/10.1111/ejn.13702

    Article  PubMed  Google Scholar 

  31. Moss CF, Surlykke A (2010) Probing the natural scene by echolocation in bats. Front Behav Neurosci. https://doi.org/10.3389/fnbeh.2010.00033

    Article  PubMed  PubMed Central  Google Scholar 

  32. Moss CF, Bohn K, Gilkenson H, Surlykke A (2006) Active listening for spatial orientation in a complex auditory scene. PLoS Biol 4(4):615–626. https://doi.org/10.1371/journal.pbio.0040079

    Article  CAS  Google Scholar 

  33. Nelson ME, MacIver MA (2006) Sensory acquisition in active sensing systems. J Comp Physiol A 192(6):573–586. https://doi.org/10.1007/s00359-006-0099-4

    Article  CAS  Google Scholar 

  34. Neuweiler G (1990) Auditory adaptations for prey capture in echolocating bats. Physiol Rev 70(3):615–641

    Article  CAS  PubMed  Google Scholar 

  35. Petrites AE, Eng OS, Mowlds DS, Simmons JA, DeLong CM (2009) Interpulse interval modulation by echolocating big brown bats (Eptesicus fuscus) in different densities of obstacle clutter. J Comp Physiol A 195(6):603–617. https://doi.org/10.1007/s00359-009-0435-6

    Article  Google Scholar 

  36. Rankin S, Oswald JN, Simonis AE, Barlow J (2015) Vocalizations of the rough-toothed dolphin, Steno bredanensis, in the Pacific Ocean. Mar Mammal Sci 31(4):1538–1548. https://doi.org/10.1111/mms.12226

    Article  Google Scholar 

  37. Roverud RC, Grinnell AD (1985a) Discrimination performance and echolocation signal integration requirements for target detection and distance determination in the CF/FM Bat Noctilio-Albiventris. J Comp Physiol A 156(4):447–456. https://doi.org/10.1007/Bf00613969

    Article  Google Scholar 

  38. Roverud RC, Grinnell AD (1985b) Echolocation sound features processed to provide distance information in the CF/FM Bat, Noctilio-Albiventris—evidence for a gated time window utilizing both CF and FM components. J Comp Physiol A 156(4):457–469. https://doi.org/10.1007/Bf00613970

    Article  Google Scholar 

  39. Sändig S, Schnitzler HU, Denzinger A (2014) Echolocation behaviour of the big brown bat (Eptesicus fuscus) in an obstacle avoidance task of increasing difficulty. J Exp Biol 217(16):2876–2884. https://doi.org/10.1242/jeb.099614

    Article  PubMed  Google Scholar 

  40. Shin YS, Chang WD, Park J, Im CH, Lee SI, Kim IY, Jang DP (2015) Correlation between inter-blink interval and episodic encoding during movie watching. PLoS One. https://doi.org/10.1371/journal.pone.0141242

    Article  PubMed  PubMed Central  Google Scholar 

  41. Shultz S, Klin A, Jones W (2011) Inhibition of eye blinking reveals subjective perceptions of stimulus salience. Proc Natl Acad Sci USA 108(52):21270–21275. https://doi.org/10.1073/pnas.1109304108

    Article  PubMed  Google Scholar 

  42. Sridharan D, Boahen K, Knudsen EI (2011) Space coding by gamma oscillations in the barn owl optic tectum. J Neurophysiol 105(5):2005–2017. https://doi.org/10.1152/jn.00965.2010

    Article  PubMed  PubMed Central  Google Scholar 

  43. Surlykke A, Ghose K, Moss CF (2009) Acoustic scanning of natural scenes by echolocation in the big brown bat Eptesicus fuscus. J Exp Biol 212(7):1011–1020. https://doi.org/10.1242/jeb.024620

    Article  PubMed  PubMed Central  Google Scholar 

  44. Turl CW, Penner RH (1989) Differences in echolocation click patterns of the beluga (Delphinapterus-Leucas) and the bottlenose dolphin (Tursiops-Truncatus). J Acoust Soc Am 86(2):497–502. https://doi.org/10.1121/1.398229

    Article  Google Scholar 

  45. Warnecke M, Falk B, Moss CF (2018) Echolocation and flight behavior of the bat Hipposideros armiger terasensis in a structured corridor. J Acoust Soc Am 144(2):806–813. https://doi.org/10.1121/1.5050525

    Article  PubMed  Google Scholar 

  46. Warnecke M, Macias S, Falk B, Moss CF (2018b) Echo interval and not echo intensity drives bat flight behavior in structured corridors. J Exp Biol https://doi.org/10.1242/jeb.191155

  47. Welker WI (1964) Analysis of sniffing of the albino rat. Behaviour 22(3/4):223–244

    Article  Google Scholar 

  48. Wesson DW, Donahou TN, Johnson MO, Wachowiak M (2008) Sniffing behavior of mice during performance in odor-guided tasks. Chem Senses 33(7):581–596. https://doi.org/10.1093/chemse/bjn029

    Article  PubMed  PubMed Central  Google Scholar 

  49. Wheeler AR, Fulton KA, Gaudette JE, Simmons RA, Matsuo I, Simmons JA (2016) Echolocating big brown bats, Eptesicus fuscus, modulate pulse intervals to overcome range ambiguity in cluttered surroundings. Front Behav Neurosci. https://doi.org/10.3389/fnbeh.2016.00125

    Article  PubMed  PubMed Central  Google Scholar 

  50. Wohlgemuth MJ, Kothari NB, Moss CF (2016) Action enhances acoustic cues for 3-D target localization by echolocating bats. PLoS Biol 14(9):1. https://doi.org/10.1371/journal.pbio.1002544

    Article  CAS  Google Scholar 

  51. Yovel Y, Falk B, Moss CF, Ulanovsky N (2010) Optimal localization by pointing off axis. Science 327(5966):701–704. https://doi.org/10.1126/science.1183310

    Article  CAS  PubMed  Google Scholar 

  52. Yovel Y, Geva-Sagiv M, Ulanovsky N (2011) Click-based echolocation in bats: not so primitive after all. J Comp Physiol A 197(5):515–530. https://doi.org/10.1007/s00359-011-0639-4

    Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Contributions

MJB performed experiments. MJB analyzed data. MJB wrote manuscript. MJB, JCH and MK conceived and directed the study. All authors discussed the results and commented on the manuscript.

Corresponding author

Correspondence to M. Jerome Beetz.

Ethics declarations

Conflict of interest

The authors declare no competing financial interests.

Ethical approval

The experiments comply with all current German laws on animal experimentation and they are in accordance with the Declaration of Helsinki. All experimental protocols were approved by the Regierungspräsidium Darmstadt (experimental permit # FU-1126).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 259 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Beetz, M.J., Kössl, M. & Hechavarría, J.C. Adaptations in the call emission pattern of frugivorous bats when orienting under challenging conditions. J Comp Physiol A 205, 457–467 (2019). https://doi.org/10.1007/s00359-019-01337-1

Download citation

Keywords

  • Bats
  • Orientation behavior
  • Active sensing
  • Sensory acquisition
  • Echolocation