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Distress calls of the greater short-nosed fruit bat Cynopterus sphinx activate hypothalamic-pituitary-adrenal (HPA) axis in conspecifics

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Abstract

In a stressful situation, greater short-nosed fruit bats (Cynopterus sphinx) emit audible vocalization either to warn or to inform conspecifics. We examined the effect of distress calls on bats emitting the call as well as the bats receiving the distress signal through analysis of the hypothalamic-pituitary-adrenal axis and catacholaminargic systems. We measured the levels of neurotransmitters [serotonin (5-HT), dopamine (DA), norepinephrine (NE)] and stress hormones [(adrenocorticotropic hormone (ACTH) and corticosterone (CORT)]. Our results showed that distress call emission elevated the level of ACTH and CORT, as well as 5-HT, DA and NE in the amygdala, for both the call emitting bat and the responding bat. Subsequently, we observed increased activity of glucocorticoid receptor and its steroid receptor co-activator (SRC-1). An expression of SRC-1 was up-regulated in the distress call emitter only, whereas it was at a similar level in both the call responder and silent bats. These findings suggest that bats emitting distress calls and also bats responding to such calls have similar neurotransmitter expression patterns, and may react similarly in response to stress.

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Abbreviations

5-HT:

5-Hydroxytryptamine (serotonin)

ACTH:

Adrenocorticotropic hormone

CORT:

Corticosterone

CRF:

Corticotrophin-releasing factor

DA:

Dopamine

GR:

Glucocorticoid receptor

NE:

Norepinephrine

RT-PCR:

Reverse transcriptase-polymerase chain reaction

SRC-1:

Steroid receptor co-activator

References

  • Adell A, Garcia-Marquez C, Armario A, Gelpi E (1988) Chronic stress increase serotonin and noradrenaline in rat brain and sensitizes their responses to a further acute stress. J Neurochem 50:1678–1681

    Article  PubMed  CAS  Google Scholar 

  • Balasingh J, Koilraj, Kunz TH (1995) Tent construction by the short-nosed fruit bat Cynopterus sphinx (Chiroptera: Pteropodidae) in southern India. Ethology 100:210-229

  • Bale TL, Lee Kuo-Fen, Vale WW (2002) The role of corticotrophin-releasing factor receptors in stress and anxiety. Integr Comp Biol 42:552–555

    Article  PubMed  CAS  Google Scholar 

  • Barlow KE, Jones G (1997) Differences in song flight calls and social calls between two phonic types of the vespertilionid bat Pipistrellus pipistrellus. J Zool (Lond) 241:315–324

    Article  Google Scholar 

  • Behr O, von Helversen O (2004) Bat serenades: complex courtship songs of the sac-winged bat (Saccopteryx bilineata). Behav Ecol Sociobiol 56:106–115

    Article  Google Scholar 

  • Belz EE, Kennell JS, Czambell RK, Rubin RT, Rhodes ME (2003) Environmental enrichment lowers stress-responsive hormones in single housed male and female rats. Pharmacol Biochem Behav 76:481–486

    Article  PubMed  CAS  Google Scholar 

  • 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: Pteropodiae). J Zool (Lond) 235:597–604

    Article  Google Scholar 

  • Bodadle-Biber MC, Singh VB, Corley KC, Phan T, Dilts RP (1993) Evidence that corticotrophin-releasing factor within the extended amygdala mediates the activation of tryptophan hydroxylase produced by sound stress in the rat. Brain Res 628:105–114

    Article  Google Scholar 

  • Bohn KM, Wilkinson GS, Moss CF (2007) Discrimination of infant isolation calls by female greater spear-nosed bats, Phyllostomus hastatus. Anim Behav 73:423–432

    Article  PubMed  Google Scholar 

  • Bohn KM, Schmidt-French B, Schwartz C, Smotherman M, Pollak GD (2009) Versatility and stereotypy of free-tailed bat songs. PLoS One 4(8):e6746

    Article  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye-binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Chaouloff F (2000) Serotonin stress and corticoids. J Psychopharmacol 14:139–151

    Article  PubMed  CAS  Google Scholar 

  • Chaverri G, Gillam EH, Vonhof MJ (2010) Social calls used by a leaf-roosting bat to signal location. Biol Lett 6:441–444

    Article  PubMed  Google Scholar 

  • Chen W, Rogatsky L, Garabendian MJ (2006) MED14 and MED1 differentially regulate target-specific gene activation by the glucocorticoid receptor. Mol Endocrinol 20:560–572

    Article  PubMed  CAS  Google Scholar 

  • Conover MR (1994) Stimuli eliciting distress calls in adult passerines and response of predators and birds to their broadcast. Behaviour 131:19–37

    Article  Google Scholar 

  • Cordero MI, Rodríguez JJ, Davies HA, Peddie CJ, Sandi C, Stewart MG (2005) Chronic restraint stress down-regulates amygdaloid expression of polysialylated neural cell adhesion molecule. Neuroscience 133:903–910

    Article  PubMed  CAS  Google Scholar 

  • Djordjević J, Cvijić G, Davidović V (2003) Different activation of ACTH and corticosterone release in response to various stressors in rats. Physiol Res 52:67–72

    PubMed  Google Scholar 

  • Dronjak S, Gavrilović L, Filipović D, Radojčić MB (2004) Immobilization and cold stress affect sympatho-adrenomedullary system and pituitary-adrenocortical axis of rats exposed to long-term isolation and crowing. Physiol Behav 81:409–415

    Article  PubMed  CAS  Google Scholar 

  • Düpjan S, Tuchscherer A, Langbein J, Schön PC, Manteuffel G, Puppe B (2011) Behavioural and cardiac responses towards conspecific distress calls in domestic pigs (Sus scrofa). Physiol Behav 103:445–452

    Article  PubMed  Google Scholar 

  • Feldman S, Weidenfeld J (1998) The excitatory effects of the amygdala on hypothalamo-pituitary-adrenocortical responses are mediated by hypothalamic norepinephrine, serotonin, and CRF-41. Brain Res Bull 45:389–393

    Article  PubMed  CAS  Google Scholar 

  • Fenton MB (1985) Communication in the chiroptera. Indiana University Press, Bloomington

    Google Scholar 

  • Ferré S, Artigas F (1993) Dopamine D2 receptor-mediated regulation of serotonin extracellular concentration in the dorsal raphe nucleus of freely moving rats. J Neurochem 61:772–775

    Article  PubMed  Google Scholar 

  • Ferré S, Cortes R, Artigas F (1994) Dopaminergic regulation of the serotonergic raphe-striatal pathway: microdialysis studies in freely moving rats. J Neurosci 14:4839–4846

    PubMed  Google Scholar 

  • Fichtel C, Hammerchmidt K (2002) Responses of redfronted lemurs to experimentally modified alarm calls: evidence for urgency-based changes in call structure. Ethology 108:763–777

    Article  Google Scholar 

  • Ganesh A, Raghuram H, Nathan PT, Marimuthu G, Rajan KE (2010) Distress call-induced gene expression in the brain of the Indian short-nosed fruit bat, Cynopterus sphinx. J Comp Physiol A 196:155–164

    Article  CAS  Google Scholar 

  • Georgiakakis P, Russo D (2012) The distinctive structure of social calls by Hanák’s dwarf bat Pipistrellus hanaki. Acta Chirop 14:167–174

    Article  Google Scholar 

  • Gervais J, Rouillard C (2000) Dorsal raphe stimulation differentially modulates dopaminergic neurons in the ventral tegmental area and substantia nigra. Synapse 35:281–291

    Article  PubMed  CAS  Google Scholar 

  • Gillam EH, Chaverri G (2011) Strong individual signatures and weaker group signatures in contact calls of spix’s disc-winged bat Thyroptera tricolor. Anim Behav 83:269–276

    Article  Google Scholar 

  • Grenhoff J, Nisell M, Ferré S, Aston-Jones G, Svensson TH (1993) Noradrenergic modulation of midbrain dopamine cell firing elicited by stimulation of the locus coerulus in the rat. J Neural Transm Gen Sec 93:11–25

    Article  CAS  Google Scholar 

  • Hajós-Korcsok K, Robinson DD, Yu JH, Fitch CS, Walker E, Merchant KM (2003) Rapid habituation of hippocampal serotonin and norepinephrine release and anxiety-related behaviors, but not plasma corticosterone levels, to repeated footshock stress in rats. Pharmacol Biochem Behav 74:609–616

    Article  PubMed  Google Scholar 

  • Hatfield E, Cacioppe JT, Rapson RL (1994) Emotional contagion. Cambridge University Press, New York

    Google Scholar 

  • Herman JP, Figueiredo H, Mueller NK, Ulrich-Lai Y, Ostrander MM, Choi DC, Cullinan WE (2003) Central mechanisms of stress integration:hierarchical circuitry controlling hypothalamo-pituitary-adrenocortical responsiveness. Front Neuroendocrinol 24:151–180

    Article  PubMed  CAS  Google Scholar 

  • Jahelková H, Horáček I, Bartonička T (2008) The advertisement song of Pipistrellus nathusii (Chiroptera, Vespertilionidae): a complex message containing acoustic signatures of individuals. Acta Chirop 10:103–126

    Article  Google Scholar 

  • Knörnschild M, von Helversen O (2008) Non-mutual vocal mother-pup recognition in the greater sac-winged bat. Anim Behav 76:1001–1009

    Article  Google Scholar 

  • Knörnschild M, Jung K, Nagy M, Metz M, Kalko EKV (2012) Bat echolocation calls facilitate social communication. Proc R Soc Lond B 279:4827–4835

    Article  Google Scholar 

  • Koenig WD, Stanback MT, Hoop PN, Mumme RL (1991) Distress call in the acorn woodpecker. Condor 93:637–643

    Article  Google Scholar 

  • Korzan WJ, Summers TR, Ronan PJ, Renner KJ, Summers CH (2001) The role of monoaminergic nuclei during aggression and sympathetic social signalling. Brain Behav Evol 57:317–327

    Article  PubMed  CAS  Google Scholar 

  • Kunz TH, Brock CE (1975) A comparison of mist-nets and ultrasonic detectors for monitoring flight activity of bats. J Mammal 56:907–911

    Article  Google Scholar 

  • Lachize S, Apostolakis EM, van der Laan S, Tijssen AM, Xu J, de Kloet ER, Meijer OC (2009) Steroid receptor coactivator-1 is necessary for regulation of corticotrophin-releasing hormone by chronic stress and glucocorticoid. Proc Natl Acad Sci USA 106:8038–8042

    Article  PubMed  CAS  Google Scholar 

  • Macedonia JM, Evans CS (1993) Essay on contemporary issues in ethology: variation among mammalian alarm call systems and the problem of meaning in animal signals. Ethology 93:177–197

    Article  Google Scholar 

  • Majzoub JA (2006) Corticotropin-releasing hormone physiology. Eur J Endocrinol 155:S71–S76

    Article  CAS  Google Scholar 

  • Makino S, Hashimoto K, Gold PW (2002) Multiple feedback mechanisms activating corticosterone-releasing hormone mRNA systems in the brain during stress. Pharmacol Biochem Behav 73:147–158

    Article  PubMed  CAS  Google Scholar 

  • McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behav 43:2–15

    Article  PubMed  Google Scholar 

  • Mohri M, Rezapoor H (2009) Effects of heprin citrate and EDTA plasma biochemistry of sheep comparison with serum. Res Vet Sci 86:111–114

    Article  PubMed  CAS  Google Scholar 

  • Morton ES (1977) On the occurrence and significance of motivation-structural rules in some bird and mammal sounds. Am Nat 111:855–869

    Article  Google Scholar 

  • Myers B, Greenwood-Van Meerveld B (2007) Corticosteroid receptor-mediated mechanisms in the amygdala regulate anxiety and colonic sensitivity. Am J Physiol Gastrointest Liver Physiol 292:G1622–G1629

    Article  PubMed  CAS  Google Scholar 

  • Nathan PT (2001). Behavior of Indian short-nosed fruit bat Cynopterus sphinx (Vahl 1797), field and semi naturalistic ethological studies. PhD Thesis, Manonmanium Sundaranar University, India

  • Nathan PT, Doss DS, Isaac SS, Balasingh J, Rajan KE, Nair NG, Subbaraj R (2001) Mist-net capture and field observations on the short-nosed fruit bat (Chiroptera: Pteropodidae) Cynopterus sphinx (Vahl). J Bombay Nat Hist Soc 98:373–378

    Google Scholar 

  • Owings DH, Morton ES (1998) Animal vocal communication: a new approach. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Pawlak R, Magarinos AM, Melchor J, McEwen B, Strickland S (2003) Tissue plasminogen activator in the amygdale is critical for stress induced anxiety-like behaviour. Nat Neurosci 6:168–174

    Article  PubMed  CAS  Google Scholar 

  • Rohwer S, Fretwell SD, Tuckfield RC (1976) Distress screams as a measure of kinship in birds. Am Midl Nat 96:418–430

    Article  Google Scholar 

  • Rosenfeld MG, Lunyak VV, Glass CK (2006) Sensors and signals: a coactivator/corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response. Genes Dev 20:1405–1428

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Seyfarth RM, Cheney DL (2003) Meaning and emotion in animal vocalizations. Ann NY Acad Sci 1000:32–55

    Article  PubMed  Google Scholar 

  • Shepard JD, Barron KW, Myers DA (2000) Corticosterone delivery to the amygdala increases corticotrophin-releasing factor mRNA in the central amygdaloid nucleus and anxiety-like behaviour. Brain Res 861:288–295

    Article  PubMed  CAS  Google Scholar 

  • Siemers BM, Kerth G (2006) Do echolocation calls of wild colony-living Bechstein’s bats (Myotis bechsteinii) provide individual-specific signature? Behav Ecol Sociobiol 59:443–454

    Article  Google Scholar 

  • Stamp JA, Herbert J (1999) Multiple immediate-early gene expression during physiological and endocrine adaptation to repeated stress. Neuroscience 94:1313–1322

    Article  PubMed  CAS  Google Scholar 

  • Stamp JA, Herbert J (2001) Corticosterone modulates autonomic responses and adaptation of central immediate-early gene expression to repeated restraint stress. Neuroscience 107:465–479

    Article  PubMed  CAS  Google Scholar 

  • Stanford SC (1996) Stress a major variable in the psychopharmacologic response. Pharmacol Biochem Behav 54:211–217

    Article  PubMed  CAS  Google Scholar 

  • Stefanski RA, Falls JB (1972a) A study of distress calls of song, swamp and white-throated sparrows (Aves: Fringillidae). 1. Interspecific responses and functions. Can J Zool 50:1501–1512

    Article  Google Scholar 

  • Stefanski RA, Falls JB (1972b) A study of distress calls of song, swamp and white-throated sparrows (Aves: Fringillidae). 2. Interspecific responses and properties used in recognition. Can J Zool 50:1513–1525

    Article  Google Scholar 

  • Storz JF, Bhat HR, Kunz TH (2000) Social structure of a polygynous tent-making bat, Cynopterus sphinx (Megachiroptera). J Zool (Lond) 251:151–165

    Article  Google Scholar 

  • Sztainberg Y, Kuperman Y, Tsoory M, Lebow M, Chen A (2010) The anxiolytic effect of environmental enrichment is mediated via amygdalar CRF receptor type 1. Mol Psychiatry 15:905–917

    Article  PubMed  CAS  Google Scholar 

  • Trainor BC (2011) Stress responses and the mesolimbic dopamine system: social contexts and sex differences. Horm Behav 60:457–469

    Article  PubMed  CAS  Google Scholar 

  • Vale W, Spiess J, Rivier C, Rivier J (1981) Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotrophin and beta-endorphin. Science 213:1394–1397

    Article  PubMed  CAS  Google Scholar 

  • van der Laan S, Lachize SB, Vreugdenhil E, de Kloet ER, Meijer OC (2008) Nuclear receptor coregulators differentially modulate induction and glucocorticoid receptor mediated repression of the corticotrophin-releasing hormone gene. Endocrinology 149:725–732

    Article  PubMed  Google Scholar 

  • Van Parijs SM, Corkeron PJ (2002) Ontogeny of vocalisations in infant black flying foxes Pteropus alecto. Behaviour 139:1111–1124

    Article  Google Scholar 

  • Waters RP, Emerson AJ, Watt MJ, Forster GL, Swallow JG, Summers CH (2005) Stress induces rapid changes in central catecholaminergic activity in Anolis carolinensis: restraint and forced physical activity. Brain Res Bull 67:210–218

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We thank M. Brock Fenton and an anonymous referee for their valuable comments and suggestions. This research was supported by Council of Scientific and Industrial Research (Grant No. 37/(1426)/10/EMR-II/2010), Government of India, through major project to KER and UGC-CAS-MKU to GM. Experimental protocol used in this study were approved by Institutional Animal Ethical Committee (03/AS/BUWAEC/2008) of Bharathidasan University and complied with the laws of India.

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Authors and Affiliations

  1. Department of Animal Science, School of Life Sciences, Bharathidasan University, Tiruchirappalli, 620024, India

    Subramanian Mariappan & Koilmani Emmanuvel Rajan

  2. Museum and Institute of Zoology, Polish Academy of Sciences, Wilcza 64, 00-679, Warszawa, Poland

    Wieslaw Bogdanowicz

  3. Department of Animal Behavior and Physiology, School of Biological Sciences, Madurai Kamaraj University, Madurai, 625021, India

    Ganapathy Marimuthu

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  1. Subramanian Mariappan
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  4. Koilmani Emmanuvel Rajan
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Correspondence to Koilmani Emmanuvel Rajan.

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Mariappan, S., Bogdanowicz, W., Marimuthu, G. et al. Distress calls of the greater short-nosed fruit bat Cynopterus sphinx activate hypothalamic-pituitary-adrenal (HPA) axis in conspecifics. J Comp Physiol A 199, 775–783 (2013). https://doi.org/10.1007/s00359-013-0838-2

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