Journal of Comparative Physiology A

, Volume 196, Issue 2, pp 155–164 | Cite as

Distress call-induced gene expression in the brain of the Indian short-nosed fruit bat, Cynopterus sphinx

  • Ambigapathy Ganesh
  • Hanumanthan Raghuram
  • Parthasarathy T. Nathan
  • Ganapathy Marimuthu
  • Koilmani Emmanuvel Rajan
Original Paper


Individuals in distress emit audible vocalizations to either warn or inform conspecifics. The Indian short-nosed fruit bat, Cynopterus sphinx, emits distress calls soon after becoming entangled in mist nets, which appear to attract conspecifics. Phase I of these distress calls is longer and louder, and includes a secondary peak, compared to phase II. Activity-dependent expression of egr-1 was examined in free-ranging C. sphinx following the emissions and responses to a distress call. We found that the level of expression of egr-1 was higher in bats that emitted a distress call, in adults that responded, and in pups than in silent bats. Up-regulated cDNA was amplified to identify the target gene (TOE1) of the protein Egr-1. The observed expression pattern Toe1 was similar to that of egr-1. These findings suggest that the neuronal activity related to recognition of a distress call and an auditory feedback mechanism induces the expression of Egr-1. Co-expression of egr-1 with Toe1 may play a role in initial triggering of the genetic mechanism that could be involved in the consolidation or stabilization of distress call memories.


Distress call Chiroptera Cynopterus sphinx egr-Toe



Immediate-early gene


Early growth response 1 gene


Target of Egr1


Postnatal day


Reverse transcriptase-polymerase chain reaction


  1. Avery MI, Racey PA, Fenton MB (1984) Short distance location of hibernaculum by little brown bats. J Zool 204:588–590CrossRefGoogle Scholar
  2. Balcombe JP, McCracken GF (1992) Vocal recognition in Mexican free-tailed bats: do pups recognize mothers? Anim Behav 43:79–88. doi:10.1016/S0003-3472(05)80073-9 CrossRefGoogle Scholar
  3. Barclay RMR, Fenton MB, Thomas DW (1979) Social behaviour of the little brown bat, Myotis lucifugus. Behav Ecol Sociobiol 6:137–146. doi:10.1007/BF00292559 CrossRefGoogle Scholar
  4. Barlow KE, Jones G (1997) Function of pipistrelle social calls: field data and a play back experiment. Anim Behav 53:991–999. doi:10.1006/anbe.1996.0398 CrossRefGoogle Scholar
  5. Bhat HR, Kunz TH (1995) Altered flower/fruit clusters of the kitul palm used as roosts by the short-nosed fruit bat, Cynopterus sphinx (Chiroptera: Pteropodidae). J Zool (Lond) 235:363–770CrossRefGoogle Scholar
  6. Boughman JW (1998) Vocal learning by greater spear-nosed bats. Proc R Soc Lond B 265:227–233CrossRefGoogle Scholar
  7. Boughman JW, Wilkinson GS (1998) Greater spear-nosed bats discriminate group mates by vocalization. Anim Behav 55:1717–1732. doi:10.1006/anbe.1997.0721 CrossRefPubMedGoogle Scholar
  8. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3 CrossRefPubMedGoogle Scholar
  9. Burmeister SS, Fernald RD (2005) Evolutionary conservation of the Egr-1 immediate-early gene response in a teleost. J Comp Neurol 481:220–232CrossRefPubMedGoogle Scholar
  10. Chamizo C, Rubio JM, Moreno J, Alvar J (2001) Semi-quantitative analysis of multiple cytokines in canine peripheral blood mononuclear cells by a single tube RT-PCR. Vet Immunol Immunopathol 83:191–202. doi:10.1016/S0165-2427(01)00385-3 CrossRefPubMedGoogle Scholar
  11. Chaudhuri A (1997) Neural activity mapping with inducible transcription factors. Neuroreport 8:5–9CrossRefGoogle Scholar
  12. Conover MR (1994) Stimuli eliciting distress call in adult passerines and response of predators and birds to their broadcast. Behavior 131:19–37CrossRefGoogle Scholar
  13. De Belle I, Wu JX, Sperandio S, Mercola D, Adamson ED (2003) In vivo cloning and characterization of a new growth suppressor protein TOE1 as a direct target gene of Egr1. J Biol Chem 278:14306–14312. doi:10.1074/jbc.M210502200 CrossRefPubMedGoogle Scholar
  14. Elangovan V, Yuvana SPE, Raghuram H, Marimuthu G (2003) Postnatal development in the Indian short-nosed fruit bat Cynopterus sphinx: growth rate and age estimation. Acta Chiropterol 5:107–116Google Scholar
  15. Esser KH, Schmidt U (1989) Mother-Infant communication in the lesser spear-nosed bat, Phyllostomus discolor (Chiroptera, Phyllostomidae): evidence for acoustic learning. Ethology 82:156–168CrossRefGoogle Scholar
  16. Fenton MB, Belwood JJ, Fullard JH, Kunz TH (1976) Responses of Myotis lucifugus (Chiroptera: Vespertilionidae) to calls of conspecifics and to other sounds. Can J Zool 54:1443–1448CrossRefGoogle Scholar
  17. Funabiki Y, Konishi M (2003) Long memory in song learning by zebra finches. J Neurosci 23:6928–6935PubMedGoogle Scholar
  18. Guzowski JF, Setlow B, Wagner EK, McGaugh JL (2001) Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268. J Neurosci 21:5089–5098. doi:0270-6474/01/215089-10$15.00/0 PubMedGoogle Scholar
  19. Jarvis ED, Nottebohm F (1997) Motor-driven gene expression. Proc Natl Acad Sci USA 94:4097–4102CrossRefPubMedGoogle Scholar
  20. Jarvis ED, Ribeiro S, Vielliard J, DaSilva M, Ventura D, Mello CV (2000) Behaviorally-driven gene expression reveals hummingbird brain vocal nuclei. Nature 406:628–632. doi:10.1038/35020570 CrossRefPubMedGoogle Scholar
  21. Jones G, Hughes PM, Rayner JMV (1991) The development of vocalizations in Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) during post-natal growth and the maintenance of individual vocal signatures. J Zool 225:71–84CrossRefGoogle Scholar
  22. Jones MW et al (2001) A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories. Nat Neurosci 4:289–296. doi:10.1038/85138 CrossRefPubMedGoogle Scholar
  23. Koenig WD, Stanback MT, Hooge PN, Mumme RL (1991) Distress calls in the acorn woodpecker. Condor 93:637–643CrossRefGoogle Scholar
  24. Kunz TH, Brock CE (1975) A comparison of mist-nets and ultrasonic detectors for monitoring flight activity of bats. J Mammal 56:907–911CrossRefGoogle Scholar
  25. Lee J, Everitt BJ, Thomas KL (2004) Independent cellular processes for hippo campal memory consolidation and reconsolidation. Science 304:839–843. doi:10.1126/science.1095760 CrossRefPubMedGoogle Scholar
  26. Liu C, Rangnekar VM, Adamson ED, Mercola D (1998) Suppression of growth and transformation and induction of apoptosis by EGR-1. Cancer Gene Ther 5:3–28PubMedGoogle Scholar
  27. Long KD, Salbaum JS (1998) Evolutionary conservation of the immediate-early gene ZENK. Mol Biol Evol 15:284–292PubMedGoogle Scholar
  28. McCaffrey TA et al (2000) High-level expression of Egr-1 and Egr-1-inducible genes in mouse and human atherosclerosis. J Clin Invest 105:653–662. doi:10.1172/JCI8592 CrossRefPubMedGoogle Scholar
  29. Mello CV, Clayton DF (1994) Song-induced ZENK gene expression in auditory pathways of songbird brain and its relation to the song control system. J Neurosci 14:6652–6666PubMedGoogle Scholar
  30. Mello CV, Velho TA, Pinaud R (2004) Song-induced gene expression: a window on song auditory processing and perception. Ann NY Acad Sci 1016:263–281CrossRefPubMedGoogle Scholar
  31. Nathan PT (2001) Behavior of Indian short nosed fruit bat Cynopterus sphinx (Vahl 1797), field and semi naturalistic ethological studies. PhD thesis, MS University, IndiaGoogle Scholar
  32. Nathan PT et al (2001) Mist-net capture and field observations on the short-nosed fruit bat (Chiroptera: Pteropodidae) Cynopterus sphinx (Vahl). J Bombay Nat Hist Soc 98:373–378Google Scholar
  33. Pascale A et al (2004) Increase of the RNA binding protein HuD and post transcriptional up-regulation of the GAP-43 gene during spatial memory. Proc Natl Acad Sci USA 101:1217–1222CrossRefPubMedGoogle Scholar
  34. Perkel DJ (2004) Origin of the anterior forebrain pathway. Ann NY Acad Sci 1016:736–748CrossRefPubMedGoogle Scholar
  35. Pfalzer G, Kusch J (2003) Structure and variability of bat social calls: implications for specificity and individual recognition. J Zool 261:21–33. doi:10.1017/S0952836903003935 CrossRefGoogle Scholar
  36. Raghuram H, Gopukumar N, Sripathi K (2007) Presence of single as well as double clicks in the echolocation signals of a fruit bat, Rousettus leschenaulti (Chiroptera: Pteropodidae). Folia Zool 56:33–38Google Scholar
  37. Routtenberg A, Rekart JL (2005) Post-translational protein modification as the substrate for long-lasting memory. Trends Neurosci 28:12–19. doi:10.1016/j.tins.2004.11.006 CrossRefPubMedGoogle Scholar
  38. 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 161:899–913CrossRefPubMedGoogle Scholar
  39. Russ JM, Jones G, Racey PA (1998) Intraspecific responses to distress calls of the pipistrelle bat, Pipistrellus pipistrellus. Anim Behav 55:705–713. doi:10.1006/anbe.997.0665 CrossRefPubMedGoogle Scholar
  40. Russ JM, Jones G, Mackie IJ, Racey PA (2004) Interspecific responses to distress calls in bats (Chiroptera: Vespertilionidae): a function for convergence in call design? Anim Behav 67:1005–1014. doi:10.1016/j.anbehav.2003.09.003 CrossRefGoogle Scholar
  41. Ryan MJ, Clark DB, Lackey JA (1985) Response of Artibeus lituratus (Chiroptera: Phyllostomidae) to distress calls of conspecifics. J Mammal 66:179–181CrossRefGoogle Scholar
  42. Smotherman M, Metzner W (2003) Effects of echo intensity on Doppler-shift compensation behavior in horseshoe bats. J Neurophysiol 89:814–821. doi:10.1152/jn.00246.2002 CrossRefPubMedGoogle Scholar
  43. Suthers RA, Summers CA (1980) Behavioural audiogram and masked thresholds of the megachiropteran echolocation bat, Rousettus. J Comp Physiol 136:223–227CrossRefGoogle Scholar
  44. Tronson NC, Taylor JR (2007) Molecular mechanisms of memory consolidation. Nat Rev Neurosci 8:262–275CrossRefPubMedGoogle Scholar
  45. Van Parijs SM, Corkeron PJ (2002) Ontogeny of vocalisations in infant black flying foxes, Pteropus alecto. Behavior 139:1111–1124CrossRefGoogle Scholar
  46. Waters DA, Vollrath C (2003) Echolocation performance and call structure in the megachiropteran fruit-bat Rosettus aegyptiacus. Acta Chiropterol 5:209–219Google Scholar
  47. Whitney O, Johnson F (2005) Motor-induced transcription but sensory-regulated translation of ZENK in socially interactive songbirds. J Neurobiol 65:251–259. doi:10.1002/neu.20187 CrossRefPubMedGoogle Scholar
  48. Zeigler HP, Marler P (2004) Behavioral neurobiology of bird song. New York Academy of Sciences, New YorkGoogle Scholar
  49. Zhang L, Jones G, Parsons S, Liang B, Zhang S (2005) Development of vocalizations in the flat-headed bats, Tylonycteris pachypus and T. robustula (Chiroptera: Vespertilionidae). Acta Chiropterol 7:91–99CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Ambigapathy Ganesh
    • 1
  • Hanumanthan Raghuram
    • 2
  • Parthasarathy T. Nathan
    • 3
  • Ganapathy Marimuthu
    • 3
  • Koilmani Emmanuvel Rajan
    • 1
  1. 1.Department of Animal Science, School of Life SciencesBharathidasan UniversityTiruchirappalliIndia
  2. 2.Centre for Ecological Sciences, Indian Institute of ScienceBangaloreIndia
  3. 3.Department of Animal Behavior and Physiology, School of Biological SciencesMadurai Kamaraj UniversityMaduraiIndia

Personalised recommendations