Absence of Jamming Avoidance and Flight Path Similarity in Paired Bent-Winged Bats, Miniopterus Fuliginosus
Kazuma Hase*, Saori Sugihara**, Seiya Oka***, and Shizuko Hiryu***
*Graduate School of Environmental Studies, Nagoya University
Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan
**Graduate School of Life and Medical Sciences, Doshisha University
1-3 Tatara-miyakodani, Kyotanabe, Kyoto 610-0321, Japan
***Faculty of Life and Medical Sciences, Doshisha University
1-3 Tatara-miyakodani, Kyotanabe, Kyoto 610-0321, Japan
Echolocating bats perceive their surroundings by listening to the echoes of self-generated ultrasound pulses. When multiple conspecifics fly in close proximity to each other, sounds emitted from nearby individuals could mutually interfere with echo reception. Many studies suggest that bats employ frequency shifts to avoid spectral overlap of pulses with other bats. Technical constraints in recording technology have made it challenging to capture subtle changes in the pulse characteristics of bat calls. Therefore, how bats change their behavior to extract their own echoes in the context of acoustic interference remains unclear. Also, to our best knowledge, no studies have investigated whether individual flight paths change when other bats are present, although movements likely reduce acoustic masking. Here, we recorded the echolocation pulses of bats flying alone or in pairs using telemetry microphones. Flight trajectories were also reconstructed using stereo camera recordings. We found no clear tendency to broaden individual differences in the acoustic characteristics of pulses emitted by pairs of bats compared to bats flying alone. However, some bats showed changes in pulse characteristics when in pairs, which suggests that bats can recognize their own calls based on the initial differences in call characteristics between individuals. In addition, we found that the paired bats spend more time flying in the same directions than in the opposite directions. Besides, we found that the flight paths of bats were more similar in “paired flight trials” than in virtual pairs of paired flight trials. Our results suggest that the bats tend to follow the other bat in paired flight. For the following bat, acoustic interference may be reduced, while the opportunity to eavesdrop on other bats’ calls may be increased.
-  J. A. Simmons, “The resolution of target range by echolocating bats,” J. Acoust. Soc. Am., Vol.54, No.1, pp. 157-173, doi: 10.1121/1.1913559, 1973.
-  N. I. Hristov, M. Betke, D. E. H. Theriault, A. Bagchi, and T. H. Kunz, “Seasonal variation in colony size of Brazilian free-tailed bats at Carlsbad Cavern based on thermal imaging,” J. Mammal., Vol.91, No.1, pp. 183-192, doi: 10.1644/08-MAMM-A-391R.1, 2010.
-  D. K. N. Dechmann, B. Kranstauber, D. Gibbs, and M. Wikelski, “Group hunting – A reason for sociality in molossid bats?,” PLoS One, Vol.5, No.2, doi: 10.1371/journal.pone.0009012, 2010.
-  N. Cvikel et al., “Bats aggregate to improve prey search but might be impaired when their density becomes too high,” Curr. Biol., Vol.25, No.2, pp. 206-211, doi: 10.1016/j.cub.2014.11.010, 2015.
-  J. A. Simmons, “Temporal binding of neural responses for focused attention in biosonar,” J. Exp. Biol., Vol.217, No.16, pp. 2834-2843, doi: 10.1242/jeb.104380, 2014.
-  C. F. Moss and A. Surlykke, “Auditory scene analysis by echolocation in bats,” J. Acoust. Soc. Am., Vol.110, No.4, pp. 2207-2226, doi: 10.1121/1.1398051, 2001.
-  N. Ulanovsky and C. F. Moss, “What the bat’s voice tells the bat’s brain,” Proc. Natl. Acad. Sci., Vol.105, No.25, pp. 8491-8498, doi: 10.1073/pnas.0703550105, 2008.
-  E. H. Gillam, N. Ulanovsky, and G. F. McCracken, “Rapid jamming avoidance in biosonar,” Proc. R. Soc. B Biol. Sci., Vol.274, No.1610, pp. 651-660, doi: 10.1098/rspb.2006.0047, 2007.
-  E. H. Gillam and B. K. Montero, “Influence of call structure on the jamming avoidance response of echolocating bats,” J. Mammal., Vol.97, No.1, pp. 14-22, doi: 10.1093/jmammal/gyv147, 2016.
-  Y. Maitani, K. Hase, K. I. Kobayasi, and S. Hiryu, “Adaptive frequency shifts of echolocation sounds in Miniopterus fuliginosus according to the frequency-modulated pattern of jamming sounds,” J. Exp. Biol., Vol.221, No.23, p. jeb.188565, doi: 10.1242/jeb.188565, 2018.
-  K. Hase, T. Miyamoto, K. I. Kobayasi, and S. Hiryu, “Rapid frequency control of sonar sounds by the FM bat, Miniopterus fuliginosus, in response to spectral overlap,” Behav. Processes, Vol.128, doi: 10.1016/j.beproc.2016.04.017, 2016.
-  E. Takahashi, K. Hyomoto, H. Riquimaroux, Y. Watanabe, T. Ohta, and S. Hiryu, “Adaptive changes in echolocation sounds by Pipistrellus abramus in response to artificial jamming sounds,” J. Exp. Biol., Vol.217, No.16, pp. 2885-2891, doi: 10.1242/jeb.101139, 2014.
-  J. Luo and C. F. Moss, “Echolocating bats rely on audiovocal feedback to adapt sonar signal design,” Proc. Natl. Acad. Sci., Vol.114, No.41, pp. 10978-10983, doi: 10.1073/pnas.1711892114, 2017.
-  M. E. Bates, S. A. Stamper, and J. A. Simmons, “Jamming avoidance response of big brown bats in target detection,” J. Exp. Biol., Vol.211, No.1, pp. 106-113, doi: 10.1242/jeb.009688, 2008.
-  J. Tressler and M. S. Smotherman, “Context-dependent effects of noise on echolocation pulse characteristics in free-tailed bats,” J. Comp. Physiol. A, Vol.195, No.10, pp. 923-934, doi: 10.1007/s00359-009-0468-x, 2009.
-  K. Hase, Y. Kadoya, Y. Maitani, T. Miyamoto, K. I. Kobayasi, and S. Hiryu, “Bats enhance their call identities to solve the cocktail party problem,” Commun. Biol., Vol.1, No.1, pp. 1-3, doi: 10.1038/s42003-018-0045-3, 2018.
-  S. Hiryu, M. E. Bates, J. A. Simmons, and H. Riquimaroux, “FM echolocating bats shift frequencies to avoid broadcast-echo ambiguity in clutter,” Proc. Natl. Acad. Sci., Vol.107, No.15, pp. 7048-7053, doi: 10.1073/pnas.1000429107, 2010.
-  M. E. Bates and J. A. Simmons, “Effects of filtering of harmonics from biosonar echoes on delay acuity by big brown bats (Eptesicus fuscus),” J. Acoust. Soc. Am., Vol.128, No.2, pp. 936-946, doi: 10.1121/1.3459823, 2010.
-  E. Amichai, G. Blumrosen, and Y. Yovel, “Calling louder and longer: How bats use biosonar under severe acoustic interference from other bats,” Proc. R. Soc. B Biol. Sci., Vol.282, No.1821, doi: 10.1098/rspb.2015.2064, 2015.
-  S. R. Hage, T. Jiang, S. W. Berquist, J. Feng, and W. Metzner, “Ambient noise induces independent shifts in call frequency and amplitude within the Lombard effect in echolocating bats,” Proc. Natl. Acad. Sci., Vol.110, No.10, pp. 4063-4068, doi: 10.1073/pnas.1211533110, 2013.
-  P. Heil and H. Neubauer, “A unifying basis of auditory thresholds based on temporal summation,” Proc. Natl. Acad. Sci., Vol.100, No.10, pp. 6151-6156, doi: 10.1073/pnas.1030017100, 2003.
-  J. Jarvis, W. Jackson, and M. Smotherman, “Groups of bats improve sonar efficiency through mutual suppression of pulse emissions,” Front. Physiol., Vol.4, p. 140, doi: 10.3389/fphys.2013.00140, 2013.
-  A. M. Adams, K. Davis, and M. Smotherman, “Suppression of emission rates improves sonar performance by flying bats,” Sci. Rep., Vol.7, 41641, doi: 10.1038/srep41641, 2017.
-  C. Chiu, W. Xian, and C. F. Moss, “Adaptive echolocation behavior in bats for the analysis of auditory scenes,” J. Exp. Biol., Vol.212, No.9, pp. 1392-1404, doi: 10.1242/jeb.027045, 2009.
-  C. Chiu, W. Xian, and C. F. Moss, “Flying in silence: Echolocating bats cease vocalizing to avoid sonar jamming,” Proc. Natl. Acad. Sci., Vol.105, No.35, pp. 13116-13121, doi: 10.1073/pnas.0804408105, 2008.
-  A. M. Adams, A. Patricio, R. Manohar, and M. Smotherman, “Influence of signal direction on sonar interference,” Anim. Behav., Vol.155, pp. 249-256, doi: 10.1016/j.anbehav.2019.05.024, 2019.
-  S. Hiryu, Y. Shiori, T. Hosokawa, H. Riquimaroux, and Y. Watanabe, “On-board telemetry of emitted sounds from free-flying bats: Compensation for velocity and distance stabilizes echo frequency and amplitude,” J. of Comparative Physiology A, Vol.194, No.9, pp. 841-851, doi: 10.1007/s00359-008-0355-x, 2008.
-  J. R. Barchi, J. M. Knowles, and J. A. Simmons, “Spatial memory and stereotypy of flight paths by big brown bats in cluttered surroundings,” J. Exp. Biol., Vol.216, No.6, pp. 1053-1063, doi: 10.1242/jeb.073197, 2013.
-  R Core Team, “R: A Language and Environment for Statistical Computing,” R Foundation for Statistical Computing, 2019.
-  D. Bates, M. Mächler, B. Bolker, and S. Walker, “Fitting Linear Mixed-Effects Models Using lme4,” J. Stat. Softw., Vol.67, No.1, pp. 1-48, doi: 10.18637/jss.v067.i01, 2015.
-  F. John and W. Sanford, “An R Companion to Applied Regression Third Edition,” Sage Publications, 2019.
-  N. Ulanovsky, M. B. Fenton, A. Tsoar, and C. Korine, “Dynamics of jamming avoidance in echolocating bats,” Proc. R. Soc. B Biol. Sci., Vol.271, No.1547, pp. 1467-1475, doi: 10.1098/rspb.2004.2750, 2004.
-  T. Bartonička, Z. Řehák, and J. Gaisler, “Can pipistrelles, Pipistrellus pipistrellus (Schreber, 1774) and Pipistrellus pygmaeus (Leach, 1825), foraging in a group, change parameters of their signals?,” J. Zool., Vol.272, No.2, pp. 194-201, doi: 10.1111/j.1469-7998.2006.00255.x, 2007.
-  M. J. Beetz, M. Kössl, and J. C. Hechavarría, “The frugivorous bat Carollia perspicillata dynamically changes echolocation parameters in response to acoustic playback,” J. Exp. Biol., Vol.224, No.6, doi: 10.1242/jeb.234245, 2021.
-  C. Chiu, P. V. Reddy, W. Xian, P. S. Krishnaprasad, and C. F. Moss, “Effects of competitive prey capture on flight behavior and sonar beam pattern in paired big brown bats, Eptesicus fuscus,” J. Exp. Biol., Vol.213, No.19, pp. 3348-3356, doi: 10.1242/jeb.044818, 2010.
-  D. K. N. Dechmann, S. L. Heucke, L. Giuggioli, K. Safi, C. C. Voigt, and M. Wikelski, “Experimental evidence for group hunting via eavesdropping in echolocating bats,” Proc. R. Soc. B Biol. Sci., Vol.276, No.1668, pp. 2721-2728, doi: 10.1098/rspb.2009.0473, 2009.
-  A. J. Corcoran and T. J. Weller, “Inconspicuous echolocation in hoary bats (Lasiurus cinereus),” Proc. R. Soc. B Biol. Sci., Vol.285, No.1878, doi: 10.1098/rspb.2018.0441, 2018.
-  M. Taub and Y. Yovel, “Segregating signal from noise through movement in echolocating bats,” Sci. Rep., Vol.10, No.1, p. 382, doi: 10.1038/s41598-019-57346-2, 2020.
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