Stable individual differences in separation calls during early development in cats and mice

Frontiers in Zoology

Volumn 12, Issue 1, 2015, Pages

  Hudson, Robyn ^a   Rangassamy, Marylin ^b   Saldaña, Amor ^a   Bánszegi, Oxána ^a   Rödel, Heiko G ^b  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b UNIVERSITÉ PARIS 13   (France)

Author keywords

Development; Felis silvestris catus; Locomotion; Mus spicilegus; Open field test; Personality; Siblings; Vocalization

Indexed keywords

EID: 84977511196     PISSN: None     EISSN: 17429994     Source Type: Journal    
DOI: 10.1186/1742-9994-12-S1-S12     Document Type: Article

References (91)

1. Wilson DS, Clark AB, Coleman K, Dearstyne T: Shyness and boldness in humans and other animals. Trends Ecol Evol. 1994, 9: 442-446.
2. Bell AM: Future directions in behavioural syndromes research. Proc R Soc B. 2007, 274: 755-761. 10.1098/rspb.2006.0199.
3. Briffa M, Weiss AA: Animal personality. Curr Biol. 2010, 20: R912-
4. Dingemanse NJ, Wolf M: Recent models for adaptive personality differences: a review. Phil Trans R Soc Lond B. 2010, 365: 3947-3958. 10.1098/rstb.2010.0221.
5. Carere C, Maestripieri D: Animal personalties: who cares and why?. Animal personalities: behaviour, physiology, and evolution. Edited by: Carere C, Maestripieri D. 2013, Chicago and London: University of Chicago Press, 1-12.
6. Dall SRX, Houston AI, McNamara JM: The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol Lett. 2004, 7: 734-739. 10.1111/j.1461-0248.2004.00618.x.
7. Wolf M, Van Doorn GS, Leimar O, Weissing FJ: Life-history trade-offs favour the evolution of animal personalities. Nature. 2007, 447: 581-584. 10.1038/nature05835.
8. Réale D, Dingemanse N, Kazem AJN, Wright J: Evolutionary and ecological approaches to the study of personality. Phil Trans R Soc Lond B. 2010, 365: 3937-3946. 10.1098/rstb.2010.0222.
9. Gosling SD, John OP: Personality dimensions in nonhuman animals: A cross-species review. Curr Dir Psychol Sci. 1999, 8: 69-75. 10.1111/1467-8721.00017.
10. Stamps J, Groothuis TGG: The development of animal personality: relevance, concepts and perspectives. Biol Rev. 2010, 85: 301-325. 10.1111/j.1469-185X.2009.00103.x.
11. Kralj-Fišer S, Schuett W: Studying personality variation in invertebrates: why bother?. Anim Behav. 2014, 91: 41-52.
12. Müller T, Müller C: Behavioural phenotypes over the lifetime of a holometabolous insect. Frontiers in Zoology. 2015, 12 (Suppl 1): S8-
13. Uher J: Individual behavioral phenotypes: an integrative meta-theoretical framework. Why "behavioral syndromes" are not analogs of "personality". Dev Psychobiol. 2011, 53: 521-548. 10.1002/dev.20544.
14. Zipser B, Kaiser S, Sachser N: Dimensions of animal personalities in Guinea pigs. Ethology. 2013, 119: 1-13. 10.1111/eth.12015.
15. Sih A, Bell A, Johnson JC: Behavioral syndromes: An ecological and evolutionary overview. Trends Ecol Evol. 2004, 19: 372-378. 10.1016/j.tree.2004.04.009.
16. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ: Integrating animal temperament within ecology and evolution. Biol Rev. 2007, 82: 291-318.
17. Trillmich F, Groothuis TGG: Unfolding personalities: the importance of studying ontogeny. Dev Psychobiol. 2011, 53: 641-655. 10.1002/dev.20574.
18. Würz Y, Krüger O: Personality over ontogeny in zebra finches: long-term repeatable traits but unstable behavioural syndromes. Frontiers in Zoology. 2015, 12 (Suppl 1): S9-
19. Trillmich F, Hudson R: The emergence of personality in animals: The need for a developmental approach. Dev Psychobiol. 2011, 53: 505-509. 10.1002/dev.20573.
20. Han C, Dingemanse NJ: Effects of diet on the structure of animal personality. Frontiers in Zoology. 2015, 12 (Suppl 1): S5-
21. Brommer JE, Class B: The importance of genotype-by-age interactions for the development of repeatable behavior and correlated behaviors over lifetime. Frontiers in Zoology. 2015, 12 (Suppl 1): S2-
22. Rödel HG, Meyer S: Early development influences ontogeny of personality types in young laboratory rats. Dev Psychobiol. 2011, 53: 601-613. 10.1002/dev.20522.
23. Guenther A, Finkemeier MA, Trillmich F: The ontogeny of personality in the wild guinea pig. Anim Behav. 2014, 90: 131-139.
24. Bergeron P, Montiglio PO, Réale D, Humphries MM, Gimenez O, Garant D: Disruptive viability selection on adult exploratory behaviour in eastern chipmunks. J Evol Biol. 2013, 26: 766-774. 10.1111/jeb.12081.
25. Rödel HG, Zapka M, Talke S, Kornatz T, Bruchner B, Hedler C: Survival costs of fast exploration during juvenile life in a small mammal. Behav Ecol Sociobiol. 2015, 69: 205-217. 10.1007/s00265-014-1833-5.
26. Bautista A, García-Torres E, Martínez-Gómez M, Hudson R: Do newborn domestic rabbits Oryctolagus cuniculus compete for thermally advantageous positions in the litter huddle?. Behav Ecol Sociobiol. 2008, 62: 331-339. 10.1007/s00265-007-0420-4.
27. Reyes-Meza V, Hudson R, Martínez-Gómez M, Nicolás L, Rödel HG, Bautista A: Possible contribution of position in the litter huddle to long-term differences in behavioral style in the domestic rabbit. Physiol Behav. 2011, 104: 778-785. 10.1016/j.physbeh.2011.07.019.
28. Bautista A, Castelán F, Pérez-Roldán H, Martínez-Gómez M, Hudson R: Competition in newborn rabbits for thermally advantageous positions in the litter huddle is associated with individual differences in brown fat metabolism. Physiol Behav. 2013, 118: 189-194.
29. Raihani G, Rodríguez A, Saladaña A, Guarneros M, Hudson R: A proposal for assessing individual differences in behaviour during early development in the domestic cat. Appl Anim Behav Sci. 2014, 154: 48-56.
30. Hudson R, Bautista A, Reyes-Meza V, Morales Montor J, Rödel HG: The effect of siblings on early development: a potential contributor to personality differences in mammals. Dev Psychobiol. 2011, 53: 564-574. 10.1002/dev.20535.
31. Petelle MB, McCoy DE, Alejandro V, Martin JGA, Blumstein DT: Development of boldness and docility in yellow-bellied marmots. Anim Behav. 2013, 86: 1147-11154. 10.1016/j.anbehav.2013.09.016.
32. Menzies AK, Timonin ME, McGuire LP, Willis CKR: Personality variation in little brown bats. PLOS ONE. 2013, 8: e80230-10.1371/journal.pone.0080230.
33. Christensson K, Cabrera T, Christensson E, Uvnäs-Moberg K, Winberg J: Separation distress call in the human neonate in the absence of maternal body contact. Acta Pediatrica. 1995, 84: 468-474. 10.1111/j.1651-2227.1995.tb13676.x.
34. Noirot E: The onset and development of maternal behavior in rats, hamsters and mice. Adv Stud Behav. 1972, 4: 107-145.
35. Hahn ME, Lavooy MJ: A review of the methods of studies on infant ultrasound production and maternal retrieval in small rodents. Behav Genet. 2005, 35: 31-51. 10.1007/s10519-004-0854-7.
36. Schneider N, Fritzsche P: Isolation calls and retrieving behaviour in laboratory and wild-derived golden hamsters - No sign for inbreeding depression. Mamm Biol. 2011, 76: 549-554.
37. Haskins R: Effect of kitten vocalizations on maternal behavior. J Comp Physiol Psychol. 1977, 91: 830-838.
38. Špinka M, Illmann G, de Jonge F, Andersson M, Schuurman T, Jensen P: Dimensions of maternal behaviour characteristics in domestic and wild domestic crossbred sows. Appl Anim Behav Sci. 2000, 70: 99-114. 10.1016/S0168-1591(00)00151-9.
39. Lingle S, Pellis SM, Wilson WF: Interspecific variation in antipredator behaviour leads to differential vulnerability of mule deer and white-tailed deer fawns early in life. J Anim Ecol. 2005, 74: 1140-1149. 10.1111/j.1365-2656.2005.01014.x.
40. Held S, Manson G, Mendl M: Maternal responsiveness of outdoor sows from first to fourth parities. Appl Anim Behav Sci. 2006, 98: 216-233. 10.1016/j.applanim.2005.09.003.
41. Rödel HG, Landmann C, Starkloff A, Kunc HP, Hudson R: Absentee mothering - not so absent? Responses of European rabbit (Oryctolagus cuniculus) mothers to pup distress calls. Ethology. 2013, 119: 1024-1033.
42. Lingle S, Wyman MT, Kotrba R, Teichroeb LJ, Romanow CA: What makes a cry a cry? A review of infant distress vocalizations. Curr Zool. 2012, 58: 698-726.
43. Schrader L, Hamerschmidt K: Computer-aided analysis of acoustic parameters in animal vocalizations. Bioacoustics. 1997, 7: 247-265. 10.1080/09524622.1997.9753338.
44. Stoeger AS, Charlton BD, Kiratochril H, Fitch WT: Vocal cues indicte level of arousal in infant African elephant roars. J Acoust Soc Am. 2011, 130: 1700-1710. 10.1121/1.3605538.
45. Scheumann M, Roser AE, Konerding W, Bleich E, Hedrich HJ, Zimmermann E: Vocal correlates of sender-identity and arousal in the isolation calls of domestic kitten (Felis silvestris catus). Front Zool. 2012, 9: 36-49. 10.1186/1742-9994-9-36.
46. Stoeger AS, Baotic A, Li D, Charlton BD: Acoustic features indicate arousal in infant giant panda vocalizations. Ethology. 2012, 118: 1-10. 10.1111/j.1439-0310.2011.01974.x.
47. Jürgens U: The neural control of vocalization in mammals: a review. J Voice. 2009, 23: 1-10. 10.1016/j.jvoice.2007.07.005.
48. Briefer EF: Vocal expression of emotions in mammals: mechanisms of production and evidence. J Zool. 2012, 288: 1-20. 10.1111/j.1469-7998.2012.00920.x.
49. De Passillé AM, Rushen J, Martin F: Interpreting the behaviour of calves in an open-field test: a factor analysis. Appl Anim Behav Sci. 1995, 45: 201-213. 10.1016/0168-1591(95)00622-Y.
50. Ligout S, Foulquié D, Sèbe F, Bouix J, Boissy A: Assessment of sociability in farm animals: The use of arena test in lambs. Appl Anim Behav Sci. 2011, 135: 57-62. 10.1016/j.applanim.2011.09.004.
51. Hudson R, Raihani G, González D, Bautista A, Distel H: Nipple preference and contests in suckling kittens of the domestic cat are unrelated to presumed nipple quality. Dev Psychobiol. 2009, 51: 322-332. 10.1002/dev.20371.
52. Raihani G, González D, Arteaga L, Hudson R: Olfactory guidance of nipple attachment and suckling in kittens of the domestic cat: inborn and learned responses. Dev Psychobiol. 2009, 51: 662-671. 10.1002/dev.20401.
53. Prechtl HFR: Angeborene Bewegungsweisen junger Katzen. Experientia. 1952, 8: 220-221. 10.1007/BF02170717.
54. Levine MS, Hull CD, Buchwald NA: Development of motor activity in kittens. Dev Psychobiol. 1978, 13: 357-371.
55. Brown KA, Buchwald JS, Johnson JR, Mikolich DJ: Vocalization in the cat and kitten. Dev Psychobiol. 1978, 11: 559-570. 10.1002/dev.420110605.
56. Baudoin C, Busquet N, Dobson FS, Gheusi G, Féron C, Durand JL, Heth G, Patris B, Todrank J: Male-female associations and female olfactory neurogenesis with pair bonding in Mus spicilegus. Biol J Linn Soc. 2005, 84: 323-334. 10.1111/j.1095-8312.2005.00437.x.
57. Sokolov VE, Kotenkova EV, Michailenko AG: Mus spicilegus. Mamm Spec. 1998, 592: 1-6.
58. Gouat P, Féron C, Demouron S: Seasonal reproduction and delayed sexual maturity in mound-building mice Mus spicilegus. Reprod Fertil Dev. 2003, 15: 187-195. 10.1071/RD02105.
59. Rangassamy M, Dalmas M, Féron C, Gouat P, Rödel HG: Similarity of personalities speeds up reproduction in pairs of a monogamous rodent. Anim Behav. 2015, 103: 7-15.
60. Patris B, Baudoin C: A comparative study of parental care between two rodent species: implications for the mating system of the mound-building mouse Mus spicilegus. Behav Processes. 2000, 51: 35-43. 10.1016/S0376-6357(00)00117-0.
61. Branchi I, Santucci D, Alleva E: Ultrasonic vocalisation emitted by infant rodents: a tool for assessment of neurobehavioural development. Behav Brain Res. 2001, 125: 49-56. 10.1016/S0166-4328(01)00277-7.
62. Elwood RW, Keeling F: Temporal organization of ultrasonic vocalization in infant mice. Dev Psychobiol. 1982, 15: 221-227. 10.1002/dev.420150306.
63. Sih A, Bell AM, Johnson JC, Ziemba RE: Behavioral syndromes: An integrative overview. Q Rev Biol. 2004, 79: 241-277. 10.1086/422893.
64. Muciño E, Bautista A, Jímenez I, Martínez-Gómez M, Hudson RJ: Differential development of body equilibrium among littermates in the newborn rabbit. Dev Psychobiol. 2009, 51: 24-33. 10.1002/dev.20339.
65. Müller R, Schrader L: Behavioural consistency during social separation and personality in diary cows. Behaviour. 2005, 142: 1289-1306. 10.1163/156853905774539346.
66. Grandin T, Deesing MJ: Genetics and the behavior of domestic animals. 2014, San Diego, USA: Academic Press, 2
67. Blum NJ, Taubman B, Heyward RY: Maternal ratings of infant intensity and distractibility: relationship with crying duration in the second month of life. Arch Pediatr Adolesc Med. 2002, 165: 286-290.
68. van Oers K, de Jong G, van Noordwijk AJ, Kempenaers B, Drent PJ: Contribution of genetics to the study of animal personalities: a review of case studies. Behaviour. 2005, 142: 1191-1212.
69. van Oers K, Mueller J: Evolutionary genomics of animal personality. Phil Trans R Soc Lond B. 2010, 365: 3991-4000. 10.1098/rstb.2010.0178.
70. Bánszegi O, Altbäcker V, Bilkó Á: Intrauterine position influences anatomy and behavior in domestic rabbits. Physiol Behav. 2009, 98: 258-262. 10.1016/j.physbeh.2009.05.016.
71. Bautista A, Rödel HG, Monclús R, Juárez-Romero M, Cruz-Sánchez E, Martínez-Gómez M, Hudson R: Intrauterine position as a predictor of postnatal growth and survival in the rabbit. Physiol Behav. 2015, 138: 101-106.
72. Hudson R, Distel H: Fighting by kittens and piglets during suckling: what does it mean?. Ethology. 2013, 119: 353-359. 10.1111/eth.12082.
73. Hudson R: Behavioural epiphenomena revisited: reply to Skok and Škorjanc. Ethology. 2014, 120: 739-741. 10.1111/eth.12264.
74. Archer J: Tests for emotionality in rats and mice: a review. Anim Behav. 1973, 21: 205-235. 10.1016/S0003-3472(73)80065-X.
75. Smith-Gill SJ: Developmental plasticity: developmental conversion versus phenotypic modulation. Am Zool. 1983, 23: 47-55.
76. McCowan LSC, Griffith SC: Nestling activity levels during begging behaviour predicts activity level and body mass in adulthood. Peer J. 2014, 2: e566-
77. Kanda LL, Louon L, Straley K: Stability in activity and boldness across time and context in captive Siberian dwarf hamsters. Ethology. 2012, 118: 518-533. 10.1111/j.1439-0310.2012.02038.x.
78. Herde A, Eccard JA: Consistency in boldness, activity and exploration at different stages of life. BMC Ecol. 2013, 13: 49-10.1186/1472-6785-13-49.
79. Sachser N: The ability to arrange with conspecifics depends on social experiences around puberty. Physiol Behav. 1993, 53: 539-544. 10.1016/0031-9384(93)90151-5.
80. Bradbury JW, Vehrencamp SL: Principes of animal communication. 2011, Massachusetts, USA: Sinauer Associates, 2
81. Simmons AM, Popper AN, Fay RR: Acoustic communication. 2013, New York, USA: Springer
82. Branchi I, Santucci D, Vitale A, Alleva E: Ultrasonic vocalizations by infant laboratory mice: a preliminary spectrographic characterization under different conditions. Dev Psychobiol. 1998, 33: 249-256. 10.1002/(SICI)1098-2302(199811)33:3<249::AID-DEV5>3.0.CO;2-R.
83. R Core Team: R: A language and environment for statistical computing. 2014, Vienna, Austria: R Foundation for Statistical Computing, [ http://www.R-project.org ]
84. Bates D, Maechler M, Bolker B: lme4: Linear mixed-effects models using Eigen and S4. 2014, R package version 1.1-7, [ http://CRAN.R-project.org/package=lme4 ]
85. Bautista A, García-Torres E, Prager G, Hudson R, Rödel HG: Development of behavior in the litter huddle in rat pups: within- and between-litter differences. Dev Psychobiol. 2010, 52: 35-43.
86. Holm S: A simple sequential rejective multiple test procedure. Scand J Stat. 1979, 6: 65-70.
87. Zuur AF, Ieno EN, Elphick CS: A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol. 2010, 1: 3-14. 10.1111/j.2041-210X.2009.00001.x.
88. Faraway JJ: Extending the linear model with R Generalized linear, mixed effects and nonparametric regression models. 2006, Boca Raton, USA: Chapman & Hall
89. Browne WJ, Subramanian SV, Jones K, Goldstein H: Variance partitioning in multilevel logistic models that exhibit overdispersion. J Roy Stat Soc A. 2005, 168: 599-613. 10.1111/j.1467-985X.2004.00365.x.
90. Lessells CM, Boag PT: Unrepeatable repeatabilities: a common mistake. Auk. 1987, 104: 116-121. 10.2307/4087240.
91. Nakagawa K, Schielzeth H: Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev Camb Philos Soc. 2010, 85: 935-956.