Abstract
In many social species group, members share acoustically similar calls. Functional hypotheses have been proposed for call sharing, but previous studies have been limited by an inability to distinguish among these hypotheses. We examined the function of vocal sharing in female budgerigars with a two-part experimental design that allowed us to distinguish between two functional hypotheses. The social association hypothesis proposes that shared calls help animals mediate affiliative and aggressive interactions, while the password hypothesis proposes that shared calls allow animals to distinguish group identity and exclude nonmembers. We also tested the labeling hypothesis, a mechanistic explanation which proposes that shared calls are used to address specific individuals within the sender–receiver relationship. We tested the social association hypothesis by creating four–member flocks of unfamiliar female budgerigars (Melopsittacus undulatus) and then monitoring the birds’ calls, social behaviors, and stress levels via fecal glucocorticoid metabolites. We tested the password hypothesis by moving immigrants into established social groups. To test the labeling hypothesis, we conducted additional recording sessions in which individuals were paired with different group members. The social association hypothesis was supported by the development of multiple shared call types in each cage and a correlation between the number of shared call types and the number of aggressive interactions between pairs of birds. We also found support for calls serving as a labeling mechanism using discriminant function analysis with a permutation procedure. Our results did not support the password hypothesis, as there was no difference in stress or directed behaviors between immigrant and control birds.
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References
Adams DC, Anthony CD (1996) Using randomisation techniques to analyse behavioural data. Anim Behav 51:733–738
Adams DM, Balsby TJS, Bradbury JW (2009) The function of double chees in orange-fronted conures (Aratinga canicularis; Psittacidae). Behaviour 146:171–188
Baayen RH (2008) Analyzing linguistic data. Cambridge University Press, Cambridge
Baglione V, Marcos J, Canestrari D, Ekman J (2002) Direct fitness benefits of group living in a complex cooperative society of carrion crows, Corvus corone corone. Anim Behav 64:887–893
Baker MC, Cunningham MA (1985) The biology of bird-song dialects. Behav Brain Sci 8:85–100
Balsby TJS, Bradbury JW (2009) Vocal matching by orange-fronted conures (Aratinga canicularis). Behav Process 82:133–139
Balsby TJS, Momberg JV, Dabelsteen T (2012) Vocal imitation in parrots allows addressing of specific individuals in a dynamic communication network. PloS ONE 7:e49747
Balsby TJS, Scarl JC (2008) Sex-specific responses to vocal convergence and divergence of contact calls in orange-fronted conures (Aratinga canicularis). Proc R Soc Lond B 275:2147–2154
Baptista LF (1985) The functional significance of song-sharing in the white-crowned sparrow. Can J Zool 63:1741–1752
Bartlett P, Slater PJB (1999) The effect of new recruits on the flock specific call of budgerigars (Melopsittacus undulatus). Ethol Ecol Evol 11:139–147
Bates D, Maechler M, Bolker B (2013) Ime4: linear mixed-effects models using S4 classes. R package version 0.999999-2. http://cran.r-project.org/web/packages/lme4/index.html
Berg KS, Delgado S, Cortopassi KA, Beissinger SR, Bradbury JW (2012) Vertical transmission of learned signatures in a wild parrot. Proc R Soc Lond B 279:585–591
Boughman J (1997) Greater spear-nosed bats give group-distinctive calls. Behav Ecol Sociobiol 40:61–70
Bradbury JW, Cortopassi KA, Clemmons JR (2001) Geographical variation in the contact calls of orange-fronted parakeets. Auk 118:958–972
Bradbury JW, Vehrencamp SL (1998) Principles of animal communication. Sinauer Associates, Sunderland
Brittan-Powell EF, Dooling RJ, Farabaugh SM (1997) Vocal development in budgerigars (Melopsittacus undulatus): contact calls. J Comp Psychol 111:226–241
Brown ED (1985) The role of song and vocal imitation among common crows (Corvus brachyrhynchos). Z Tierpsychol 68:115–136
Brown ED, Farabaugh SM (1991) Song sharing in a group-living songbird, the Australian Magpie Gymnorhina tibicen: Part III. Sex specificity and individual specificity of vocal parts in communal chorus and duet songs. Behaviour 118:244–274
Brown ED, Farabaugh SM (1997) What birds with complex social relationships can tell us about vocal learning: vocal sharing in avian groups. In: Snowdon CT, Farabaugh SM (eds) Social influence on vocal development. Cambridge University Press, Cambridge
Brownie AC (1992) The metabolism of adrenal cortical steroids. In: James VHT (ed) The adrenal gland. Raven, NY
Caldwell MC, Caldwell DK, Tyack PL (1990) Review of the signature-whistle hypothesis for the Atlantic bottlenose dolphins. In: Leatherwood S, Reeves RR (eds) The bottlenose dolphins. Academic, New York, pp 191–234
Candiotti A, Zuberbuhler K, Lemasson A (2012) Convergence and divergence in Diana monkey vocalizations. Biol Lett 8:382–385
Charrier I, Mathevon N, Jouventin P (2001) Mother’s voice recognition by seal pups. Nature 412:873
Cheney DL, Seyfarth RM (1980) Vocal recognition in free-ranging vervet monkeys. Anim Behav 28:362–367
Cortopassi KA, Bradbury JW (2006) Contact call diversity in wild orange-fronted parakeet pairs, Aratinga canicularis. Anim Behav 71:1141–1154
Creel S (2001) Social dominance and stress hormones. Nature 379:212
D’Ettorre P, Heinze J (2005) Individual recognition in ant queens. Curr Biol 15:2170–2174
Dehnhard M, Schreer A, Krone O, Jewgenow K, Krause M, Grossman R (2003) Measurement of plasma corticosterone and fecal glucocorticoid metabolites in the chicken (Gallus domesticus), the great cormorant (Phalacrocorax carbo), and the goshawk (Accipiter gentilis). Gen Comp Endocrinol 131:345–352
Dooling RJ (1986) Perception of vocal signal by budgerigars (Melopsittacus undulatus). Exp Biol 45:195–218
Ebensperger LA, Blumstein DT (2006) Sociality in New World hystricognath rodents is linked to predators and burrow digging. Behav Ecol 12:227–236
Ebensperger LA, Ramirez-Estrada J, Leon C, Castro RA, Tolhuysen LO, Sobrero R, Quirici V, Burger JB, Soto-Gamboa M, Hayes LD (2011) Sociality, glucorticoids and direct fitness in the communally rearing rodent, Octodon degus. Horm Behav 60:346–352
Farabaugh SM, Brown ED, Veltman CJ (1988) Song sharing in a group-living songbird, the Australian Magpie Gymnorhina tibicen: Part II. Vocal sharing between territorial neighbors, within and between geographic regions, and between sexes. Behaviour 104:105–125
Farabaugh SM, Dooling RJ (1996) Acoustic communication in parrots: laboratory and field studies of Budgerigars, Melopsittacus undulatus. In: Kroodsma DE, Miller EH (eds) Ecology and evolution of acoustic communication in birds. Cornell University Press, Ithaca, pp 97–117
Farabaugh SM, Linzenbold A, Dooling RJ (1994) Vocal plasticity in budgerigars (Melopsitticus undulatus): evidence for social factors in the learning of contact calls. J Comp Psychol 108:81–92
Feekes F (1982) Song mimesis within colonies in Cacicus c. cela (Icteridae, Aves). A colonial password? Z Tierpsychol 58:119–152
Feng AS, Riede T, Arch VS, Yu Z, Zu Z, Yu X, Shen J (2009) Diversity of the vocal signals of concave-eared torrent frogs (Odorrana tormota): evidence for individual signatures. Ethology 115:1015–1028
Field A (2005) Discovering statistics using SPSS. Sage Publications, London
Fujiwara HE, Kanesada A, Okamoto Y, Satoh R, Watanabe A, Miyamoto T (2011) Long-term maintenance and eventual extinction of preference for a mate’s call in the female budgerigar. Anim Behav 82:971–979
Goymann W (2005) Non-invasive monitoring of hormones in bird droppings: physiological validation, sampling, extraction, sex differences and the influence of diet on hormone metabolite levels. Ann NY Acad Sci 1046:35–53
Goymann W, Wingfield JC (2004) Allostatic load, social status and stress hormones: the costs of social status matter. Anim Behav 67:591–602
Groth JG (1993) Call matching and positive assortative mating in red crossbills. Auk 110:398–401
Hass CC, Valenzuela D (2002) Anti-predator benefits of group living in white-nosed coatis (Nasua narica). Behav Ecol Sociobiol 51:570–578
Hile AG, Burley NT, Coopersmith CB, Foster VS, Striedter GF (2005) Effects of male vocal learning on female behavior in the budgerigar, Melopsittacus undulatus. Ethology 111:901–923
Hile AG, Plummer TK, Striedter GF (2000) Male vocal imitation produces call convergence during pair bonding in budgerigars, Melopsittacus undulatus. Anim Behav 59:1209–1218
Hile AG, Striedter GF (2000) Call convergence within groups of female budgerigars (Melopsittacus undulatus). Ethology 106:1105–1114
Höjesjö J, Johnsson JI, Petersson E, Järvi T (1998) The importance of being familiar: individual recognition and social behavior in sea trout (Salmo trutta). Behav Ecol 9:445–451
Janik VM (1999) Pitfalls in the categorization of behaviour: a comparison of dolphin whistle classification methods. Anim Behav 57:133–143
Janik VM (2000) Whistle matching in wild bottlenose dolphins (Tursiops truncatus). Science 289:1355–1357
Janik VM (2009) Acoustic communication in delphinids. Adv Stud Behav 40:123–157
Janik VM, Slater PJB (1998) Context-specific use suggests that bottlenose dolphin signature whistles are cohesion calls. Anim Behav 56:829–838
Janik VM, Slater PJB (2000) The different roles of social learning in vocal communication. Anim Behav 60:1–11
Keenan PC, Benkman CW (2008) Call imitation and call modification in red crossbills. Condor 110:93–101
Kershenbaum A, Llany A, Blaustein L, Geffen G (2012) Syntactic structure and geographical dialects in the songs of male rock hyraxes. Proc R Soc Lond B 279:2974–2981
King SL, Sayigh LS, Wells RS, Fellner W, Janik VM (2013) Vocal copying of individually distinctive signature whistles in bottlenose dolphins. Proc R Soc Lond B 280
Kirschel ANG, Cody ML, Harlow ZT, Promponas VJ, Tayloer EE, Tayloer CE (2011) Territorial dynamics of Mexican Ant-thrushes Formicarius moniliger revealed by individual recognition of their songs. Ibis 153:255–268
Kondo N, Izawa EI, Watanabe S (2010) Perceptual mechanism for vocal individual recognition in jungle crows (Corvus macrorhynchos): contact call signature and discrimination. Behaviour 147:1051–1072
Lahaye SEP, Eens M, Darras VM, Pinxten R (2012) Testosterone stimulates the expression of male-typical socio-sexual and song behaviors in female budgerigars (Melopsittacus undulatus): an experimental study. Gen Comp Endocrinol 178:82–88
Lemasson A, Gautier J, Hausberger M (2003) Vocal similarities and social bonds in Campbell’s money (Cercopithecus Campbelli). Ethology 326:1185–1193
Lengagne T (2001) Temporal stability in the individual features in the calls of eagle owls (Bubo bubo). Behaviour 138:1407–1419
Lougheed SC, Handford P (1992) Vocal dialects and the structure of geographic variation in the morphological and allozymic characters in the rufous-collared sparrow, Zonotrichia capensis. Evolution 46:1443–1456
Mammen DL, Nowicki S (1981) Individual differences and within-flock convergence in chickadee calls. Behav Ecol Sociobiol 9:179–186
Manly BFJ (1997) Randomization, bootstrap and Monte Carlo methods in biology. Chapman & Hall, New York
McComb K, Moss C, Sayialel S, Baker L (2000) Unusually extensive networks of vocal recognition in African elephants. Anim Behav 59:1103–1109
Miller PJO, Shapiro AD, Tyack PL, Solow AR (2004) Call-type matching in vocal exchanges of free-ranging killer whales, Orcinus orca. Anim Behav 67:1099–1107
Mitani JC, Brandt KL (1994) Social factors influence the acoustic variability in the long-distance calls of male chimpanzees. Ethology 96:233–252
Mitani JC, Watts DPaL, JS (2002) Ecological and social correlates of chimpanzee party size and composition. In: Boesch C, Lohmann G, Marchant LL (eds) Behavioural diversity in chimpanzees and bonobos. Cambridge Univeristy Press, Cambridge, UK, pp 102–111
Mooring MS, Hart BL (1992) Animal grouping for protection from parasites: selfish herd and encounter-dilution effects. Behaviour 123:173–193
Moravec ML, Striedter GF (2010) “Virtual parrots” confirm mating preferences of female budgerigars. Ethology 116:961–971
Moravec ML, Striedter GF, Burley NT (2006) Assortative pairing based on contact call similarity in budgerigars, Melopsittacus undulatus. Ethology 112:1108–1116
Möstl E, Rettenbacher S, Palme R (2005) Measurement of corticosterone metabolites in birds’ droppings: an analytical approach. Ann NY Acad Sci 1046:17–34
Mundinger PC (1970) Vocal imitation and individual recognition of finxh calls. Science 168:480–482
Mundry R, Sommer C (2007) Discriminant function analysis with nonindependent data: consequences and an alternative. Anim Behav 74:965–976
Myasato LE, Baker MC (1999) Black-capped chickadee call dialects along a continuous habitat corridor. Anim Behav 6:1311–1318
Nousek AE, Slater PJB, Wang C, Miller PJO (2006) The influence of social affiliation on individual vocal signatures of northern resident killer whales (Orcinus orca). Biol Lett 22:481–484
Nowicki S, Nelson DA (2010) Defining natural categories in acoustic signals: comparison of three methods applied to ‘chick-a-dee’ call notes. Ethology 86:89–101
O’Brien TG (1991) Female–male social interactions in wedge-capped capuchin monkeys: benefits and costs of group living. Anim Behav 41:555–567
Pease SM, Salina-Melgoza A, Escalante P, Renton K, Wright TF (2012) Offspring sex ratios in the lilac-crowned parrot (Amazona finschi). Wilson J Ornithol 124:393–396
Price JJ (2003) Communication with shared call repertoires in the cooperatively breeding stripe-backed wren. J Field Ornithol 74:166–171
Quinn GP, Keough MJ (2002) Experimental designs and data analysis for biologists. Cambridge University Press, Cambridge
R Development Core Team (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Rendall D, Rodman PS, Emond RE (1996) Vocal recognition of individuals and kin in free-ranging rhesus monkeys. Anim Behav 51:1007–1015
Salinas-Melgoza A, Wright TF (2012) Vocal learning and limited dispersal as dual mechanisms for dialect maintenance in a parrot. PLoS ONE 7:e48667
Saltzman W, Schulz-Darken NJ, Scheffler G, Wegner FH, Abbott DH (1994) Social and reproductive influences on plasma cortisol in female marmoset monkeys. Physiol Behav 56:801–810
Sapolsky RM (1987) Stress, social status, and reproductive physiology in free-living baboons. Prentice-Hall, Englewood Cliffs
Sayigh LS, Esch HC, Janik VM (2007) Facts about signature whistles of bottlenose dolphins (Tursiops truncatus). Anim Behav 74:1631–1642
Sayigh LS, Tyack PL, Wells RS, Scott MD (1990) Signature whistles of free-ranging bottlenosed dolphins, Tursiops truncatus: stability and mother-offspring comparisons. Behav Ecol Sociobiol 26:247–260
Scarl JC, Bradbury JW (2009) Rapid vocal convergence in an Australian cockatoo, the galah Eolophus roseicapillus. Anim Behav 77:1019–1026
Searcy WA, Beecher MD (2009) Song as an aggressive signal in songbirds. Anim Behav 78:1281–1292
Sewall KS (2009) Limited adult vocal learning maintains call dialects but permits pair-distinctive calls in red crossbills. Anim Behav 77:1303–1311
Silva APD, Stam A (1996) Discriminant Analysis. In: Grimm LG, Yarnold PR (eds) Reading and understanding multivariate statistics. American Psychological Association, Washington, pp 277–318
Slater JB (1989) Bird song learning: causes and consequences. Ethol Ecol Evol 1:19–46
Smolker R, Pepper JW (1999) Whistle convergence among allied male bottlenose dolphins (Delphinidae, Tursiops sp.). Ethology 105:595–617
Sokal RR, Rohlf FJ (1995) Biometry—the principles and practice of statistics in biological research. Freeman, New York
Stiles GF (1979) Ecology and evolution of lek mating ehavior in the long-tailed hermit hummingbird. Ornithol Monogr 27:1–74
Striedter GF, Freibott L, J Höjesjö AG, Burley NT (2003) For whom the male calls: an effect of audience on contact call rate and repertoire in budgerigars, Melopsittacus undulatus. Anim Behav 65:875–882
Tabachnick BG, Fidell LS (2001) Using multivariate statistics. Allyn & Bacon, Boston
Tchernichovski O, Nottebohm F, Ho CE, Bijan P, Mitra PP (2000) A procedure for an automated measurement of song similarity. Anim Behav 59:1167–1176
Tibbetts EA (2002) Visual signals of individual identity in the wasp Polistes fuscatus. Proc R Soc Lond B 269:1423–1428
Touma C, Palme R (2005) Measuring fecal glucorticoid metabolites in mammals and birds: the importance of validation. Ann NY Acad Sci 1046:54–74
Tyack P (2008) Convergence of calls as animals form social bonds, active compensation for noisy communication channels, and the evolution of vocal learning in mammals. J Comp Psychol 122:319–331
Tyack PL (1997) Development and social functions of signature whistles in bottlenose dolphins Tursiops truncatus. Bioacoustics 8:21–46
Tyack PL (2000a) Dolphins whistle a signature tune. Anim Behav 289:1310–1311
Tyack PL (2000b) Functional aspects of cetacean communication. In: Mann J, Connor RC, Tyack PL, Whitehead H (eds) Field studies of dolphins and whales. University of Chicago Press, Chicago, pp 270–307
Tyack PL (2003) Dolphins communicate about individual-specific social relationships. In: De Waal FBM, Tyack PL (eds) Animal social complexity, intelligence and individualized societies. Harvard University Press, Cambridge
Uetz GW, Hieber CS (1997) Colonial web-building spiders: balancing the costs and benefits of group-living. In: Choe JC, Crespo BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge
Valone TJ (1989) Group foraging, public information, and patch estimation. Oikos 56:357–363
Vehrencamp SL (2001) Is song-type matching a conventional signal of aggressive intentions? Proc R Soc Lond B 268:1637–1642
Vehrencamp SL, Ritter AF, Keever M, Bradbury JW (2003) Responses to playback of local vs distant contact calls in the orange-fronted conure, Aratinga canicularis. Ethology 109:37–54
Venables WN, Ripley BD (2002) Modern Applied Statistics with S. Springer, New York
Wanker R, Apcin J, Jennerjahn B, Waibel B (1998) Discrimination of different social companions in spectacled parrotlets (Forpus conspicillatus): evidence for individual vocal recognition. Behav Ecol Sociobiol 43:197–202
Wanker R, Sugama Y, Prinage S (2005) Vocal labelling of family members in spectacled parrotlets, Forpus conspicillatus. Anim Behav 70:111–118
Watwood SL, Tyack PL, Wells RS (2004) Whistle sharing in paired male bottlenose dolphins, Tursiops truncatus. Behav Ecol Sociobiol 55:531–543
Wright TF, Dahlin CR, Salinas-Melgoza A (2008) Stability and change in vocal dialects of the yellow-naped amazon. Anim Behav 76:1017–1027
Wyndham E (1980) Diurnal cycle, behavior and social organization of the budgerigar, Melopsittacus undulatus. Emu 80:25–33
Yang X, Lei F, Wang G, Jesse A (2007) Syllable sharing and inter-individual syllable variation in Anna’s hummingbird Calypte anna songs, in San Francisco, California. Folia Zool 56:307–318
Young A (2011) Vocal learning in budgerigars, Melopsittacus undulatus: process and function. Dissertation. New Mexico State University, Las Cruces
Young A, Hallford D (2012) Validation of a fecal glucocorticoid metabolite assay to assess stress in the budgerigar (Melopsittacus undulatus). Zoo Biol 10:112–116
Yurk H, Barrett-Lennard L, Ford JKB, Matkins CO (2002) Cultural transmission within maternal lineages: vocal clans in resident killer whales in southern Alaska. Anim Behav 63:1103–1119
Acknowledgments
We thank Dr. Dennis Hallford and Chelsea Felker for conducting the FGM RIA. We gratefully acknowledge the assistance of Jim Ha who wrote the Palm Pilot program. We thank Anna Berglund and Josh Criswell for assistance with recording the budgerigars and fecal processing. We thank Alfredo Montoya and the staff of the New Mexico State University Animal Care Facility for maintaining our population of budgerigars and providing laboratory space. We also thank Shannon Pease and Daniel Acosta for assistance with genetic sexing. Additional thanks go to Chelsea Blake and Amy Dundorf for assistance with randomized call sorting. We also thank two anonymous reviewers and Dr. Henrik Brumm for insightful comments that improved the quality of the manuscript. Funding was provided to T.W. by NICHD grant SC1HD068128 and a New Mexico State University Arts and Sciences mini-grant.
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Our experiments comply with the current laws of the USA and were approved by the New Mexico State University IACUC (protocol number 2010–001).
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Dahlin, C.R., Young, A.M., Cordier, B. et al. A test of multiple hypotheses for the function of call sharing in female budgerigars, Melopsittacus undulatus . Behav Ecol Sociobiol 68, 145–161 (2014). https://doi.org/10.1007/s00265-013-1631-5
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DOI: https://doi.org/10.1007/s00265-013-1631-5