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PloS one2020; 15(4); e0231343; doi: 10.1371/journal.pone.0231343

Communication is key: Mother-offspring signaling can affect behavioral responses and offspring survival in feral horses (Equus caballus).

Abstract: Acoustic signaling plays an important role in mother-offspring recognition and subsequent bond-formation. It remains unclear, however, if mothers and offspring use acoustic signaling in the same ways and for the same reasons throughout the juvenile stage, particularly after mutual recognition has been adequately established. Moreover, despite its critical role in mother-offspring bond formation, research explicitly linking mother-infant communication strategies to offspring survival are lacking. We examined the communicative patterns of mothers and offspring in the feral horse (Equus caballus) to better understand 1) the nature of mother-offspring communication throughout the first year of development; 2) the function(s) of mother- vs. offspring-initiated communication and; 3) the importance of mare and foal communication to offspring survival. We found that 1) mares and foals differ in when and how they initiate communication; 2) the outcomes of mare- vs. foal-initiated communication events consistently differ; and 3) the communicative patterns between mares and their foals can be important for offspring survival to one year of age. Moreover, given the importance of maternal activity to offspring behavior and subsequent survival, we submit that our data are uniquely positioned to address the long-debated question: do the behaviors exhibited during the juvenile stage (by both mothers and their young) confer delayed or immediate benefits to offspring? In summary, we aimed to better understand 1) the dynamics of mother-offspring communication, 2) whether mother-offspring communicative patterns were important to offspring survival, and 3) the implications of our research regarding the function of the mammalian juvenile stage. Our results demonstrate that we have achieved those aims.
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Publication Date: 2020-04-17 PubMed ID: 32302348PubMed Central: PMC7164835DOI: 10.1371/journal.pone.0231343Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research explores the importance of acoustic communication between mother horses and their offspring for survival and behavioral responses, specifically during the first year of development. It aims to understand the different communication patterns and their implications for the offspring’s survival and the broader significance for juvenile mammalian behavior.

Understanding Mother-Offspring Communication

  • The researchers investigated the communicative patterns of mother-offspring in feral horses.
  • Specifically, they focused on the first year of development, which is an important period for forming bonds and recognizing each other.
  • The query is if this acoustic signaling stays the same after this mutual recognition, since it’s unclear whether the patterns remain constant or change over time.

Communication Initiation and Consequences

  • The research further delves into who initiates communication—mare or foal—and the outcomes of their communication tactics.
  • The results show that mother horses (mares) and their young (foals) differ in when and how they initiate communication.
  • It also shows disparities between mare- and foal-initiated communication events: they consistently have different outcomes.

Linking Communication to Offspring Survival

  • A significant aspect of this research is linking mother-infant communication strategies with offspring survival, a domain that hasn’t been considerably explored before.
  • The researchers found that the communication patterns between mares and their foals can be crucial for the survival of the young up to one year of age.

Implications for Juvenile Behaviour

  • The study argues that their data can contribute to the long-standing question of whether behaviors exhibited during the juvenile stage by mothers and their young have immediate or delayed benefits to the offspring.
  • It does this by analyzing the effect of the mother’s activity on offspring behavior and, consequently, their survival.

Cite This Article

APA
Nuñez CMV, Rubenstein DI. (2020). Communication is key: Mother-offspring signaling can affect behavioral responses and offspring survival in feral horses (Equus caballus). PLoS One, 15(4), e0231343. https://doi.org/10.1371/journal.pone.0231343

Publication

PloS one
ISSN: 1932-6203
NlmUniqueID: 101285081
Country: United States
Language: English
Volume: 15
Issue: 4
Pages: e0231343
PII: e0231343

Researcher Affiliations

Nuñez, Cassandra M V
  • Department of Biological Sciences, The University of Memphis, Memphis, Tennessee, United States of America.
  • Department of Natural Resource Ecology and Management, Iowa State University, Ames, Iowa, United States of America.
  • Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, United States of America.
Rubenstein, Daniel I
  • Department of Ecology and Evolutionary Biology, Princeton University, Princeton, New Jersey, United States of America.

MeSH Terms

  • Animal Communication
  • Animals
  • Behavior, Animal / physiology
  • Female
  • Horses

Conflict of Interest Statement

The authors have declared that no competing interests exist.

References

This article includes 65 references
  1. Mogi K, Takakuda A, Tsukamoto C, Ooyama R, Okabe S, Koshida N, Nagasawa M, Kikusui T. Mutual mother-infant recognition in mice: The role of pup ultrasonic vocalizations.. Behav Brain Res 2017 May 15;325(Pt B):138-146.
    doi: 10.1016/j.bbr.2016.08.044pubmed: 27567527google scholar: lookup
  2. Nowak R, Keller M, Lévy F. Mother-young relationships in sheep: a model for a multidisciplinary approach of the study of attachment in mammals.. J Neuroendocrinol 2011 Nov;23(11):1042-53.
    doi: 10.1111/j.1365-2826.2011.02205.xpubmed: 21827554google scholar: lookup
  3. Okabe S, Nagasawa M, Mogi K, Kikusui T. Importance of mother-infant communication for social bond formation in mammals.. Anim Sci J 2012 Jun;83(6):446-52.
    doi: 10.1111/j.1740-0929.2012.01014.xpubmed: 22694327google scholar: lookup
  4. Elwood RW, Keeling F. Temporal organization of ultrasonic vocalizations in infant mice.. Dev Psychobiol 1982 May;15(3):221-7.
    doi: 10.1002/dev.420150306pubmed: 7095288google scholar: lookup
  5. Banszegi O, Szenczi P, Urrutia A, Hudson R. Conflict or consensus? Synchronous change in mothere-young vocal communication across weaning in the cat.. Animal Behaviour 2017;130:233–40.
  6. Kikusui T, Isaka Y, Mori Y. Early weaning deprives mouse pups of maternal care and decreases their maternal behavior in adulthood.. Behav Brain Res 2005 Jul 30;162(2):200-6.
    doi: 10.1016/j.bbr.2005.03.013pubmed: 15970216google scholar: lookup
  7. Kikusui T, Takeuchi Y, Mori Y. Early weaning induces anxiety and aggression in adult mice.. Physiol Behav 2004 Mar;81(1):37-42.
    pubmed: 15059682doi: 10.1016/j.physbeh.2003.12.016google scholar: lookup
  8. Bateson P, Young M. Separation from the mother and the development of play in cats.. Animal Behaviour 1981;29(1):173–80.
  9. Fagen RM. Animal play behavior.. New York, NY: Oxford University Press; 1981.
  10. Gomendio M. The development of different types of play in gazelles: Implications for the nature and functions of play.. Animal Behaviour 1988;36(3):825–36.
  11. Lee PC. Play as a means for developing relationships. In: Hinde RA, editor. Primate social relationships. Oxford, UK: Blackwell Science Ltd.; 1983. p. 82–9.
  12. Martin P, Caro TM. On the functions of play and its role in behavioral development.. Advances in the Study of Behavior 1985;15:59–103.
  13. Cameron EZ, Linklater WL. Individual mares bias investment in sons and daughters in relation to their condition.. Anim Behav 2000 Sep;60(3):359-367.
    doi: 10.1006/anbe.2000.1480pubmed: 11007645google scholar: lookup
  14. Tyler SJ. The behaviour and social organization of the New Forest ponies.. Animal Behaviour Monographs 1972;5:85–196.
  15. Feist JD, McCullough DR. Behavior patterns and communication in feral horses.. Z Tierpsychol 1976 Aug;41(4):337-71.
    doi: 10.1111/j.1439-0310.1976.tb00947.xpubmed: 983427google scholar: lookup
  16. Linklater WL, Cameron EZ, Stafford KJ, Veltman CJ. Social and spatial structure and range use by Kaimanawa wild horses (Equus caballus: Equidae).. New Zealand Journal of Ecology 2000;24(2):139–52.
  17. Rubenstein DI. Behavioural ecology of island feral horses.. Equine Veterinary Journal 1981;13(1):27–34.
  18. Klingel H. Social organization and reproduction in equids.. J Reprod Fertil Suppl 1975 Oct;(23):7-11.
    pubmed: 1060868
  19. Cameron EZ, Setsaas TH, Linklater WL. Social bonds between unrelated females increase reproductive success in feral horses.. Proc Natl Acad Sci U S A 2009 Aug 18;106(33):13850-3.
    doi: 10.1073/pnas.0900639106pmc: PMC2728983pubmed: 19667179google scholar: lookup
  20. Stanley CR, Mettke-Hofmann C, Hager R, Shultz S. Social stability in semiferal ponies: networks show interannual stability alongside seasonal flexibility.. Animal Behaviour 2018;136:175–84.
  21. Nuñez CMV. Mother-young relationships in feral horses (Equus caballus): Implications for the function of development in mammals.. Princeton, NJ, USA: nhttp://search.proquest.com/pqdtft/advanced?accountid=13314: Princeton University; 2000.
  22. Feh C. Relationships and communication in socially natural horse herds. The Domestic Horse: The Origins, Development and Management of Its Behaviour: Cambridge University Press; 2005. p. 83–93.
  23. Waring GH. Horse behavior.. Second ed Norwich, NY, USA: Noyes Publications/William Andrew Publishing; 2003. 442 p.
  24. Yeon SC. Acoustic communication in the domestic horse (Equus caballus).. Journal of Veterinary Behavior 2012;7(3):179–85.
  25. Schwartz JJ, Bee MA. Anuran acoustic signal production in noisy environments. In: Brumm H, editor. Animal Communication and Noise Berlin, Germany: Springer; 2013. p. 91–132.
  26. Brumm H, Zollinger SA. Avian vocal production in noise. In: Brumm H, editor. Animal Communication and Noise. Berlin, Germany: Springer; 2013. p. 187–227.
  27. Quam RM, Ramsier MA, Fay RR, Popper AN. Primate Hearing and Communication.. Quam RM, Ramsier MA, Fay RR, Popper AN, editors. Cham, Switzerland: Springer International Publishing; 2017.
  28. Tyack P, Janik VM. Effects of noise on acoustic signal production in marine animals. In: Brumm H, editor. Animal Communication and Noise Berlin, Germany:: Springer; 2013. p. 251–71.
  29. Lampe U, Schmoll T, Franzke A, K R. Staying tuned: Grasshoppers from noisy roadside habitats produce courtship signals with elevated frequency components.. Functional Ecology 2012;26:1348–54.
  30. Crowell-Davis SL. Nursing behaviour and maternal aggression among Welsh ponies (Equus caballus).. Applied Animal Behaviour Science 1985;14(1):11–25.
  31. Crowell-Davis SL. Spatial relations between mares and foals of the Welsh pony (Equus caballus).. Animal Behaviour 1986;34(4):1007–15.
  32. Altmann J. Baboon Mothers and Infants:. University of Chicago Press; 2001.
  33. Byers JA. Animal play: Evolutionary, comparative and ecological perspectives.. Cambridge: Cambridge University Press; 1998.
  34. Conant EK, Juras R, Cothran EG. A microsatellite analysis of five Colonial Spanish horse populations of the southeastern United States.. Anim Genet 2012 Feb;43(1):53-62.
    doi: 10.1111/j.1365-2052.2011.02210.xpubmed: 22221025google scholar: lookup
  35. Linklater WL, Cameron EZ. Tests for cooperative behaviour between stallions.. Anim Behav 2000 Dec;60(6):731-743.
    doi: 10.1006/anbe.2000.1525pubmed: 11124871google scholar: lookup
  36. Rubenstein DI. Ecology and sociality in horses and zebras. In: Rubenstein DI, Wrangham R.W., editor. Ecological Aspects of Social Evolution, Birds and Mammals. Princeton: Princeton University Press; 1986. p. 282–302.
  37. Feh C. Alliances and reproductive success in Camargue stallions.. Anim Behav 1999 Mar;57(3):705-713.
    doi: 10.1006/anbe.1998.1009pubmed: 10196062google scholar: lookup
  38. Pacheco MA, Herrera EA. Social structure of feral horses in the llanos of Venezuela.. Journal of Mammalogy 1997;78(1):15.
  39. Rubenstein DI, Nuñez CMV. Sociality and reproductive skew in horses and zebras. In: Hager R, Jones CB, editors. Reproductive Skew in Vertebrates: Proximate and Ultimate Causes. Cambridge: Cambridge University Press; 2009. p. 196–226.
  40. National Park Service. Cape Lookout NS (CALO) Special Report.. https://irma.nps.gov/Stats/SSRSReports/Park%20Specific%20Reports/Park%20YTD%20Version%202?Park=CALO 2018.
  41. Altmann J. Observational study of behavior: sampling methods.. Behaviour 1974;49(3):227-67.
    pubmed: 4597405doi: 10.1163/156853974x00534google scholar: lookup
  42. Kiley-Worthington M. The Behaviour of Horses in Relation to Management and Training.. London: J.A. Allen; 1987.
  43. Stomp M, Leroux M, Cellier M, Henry S, Lemasson A, Hausberger M. An unexpected acoustic indicator of positive emotions in horses.. PLoS One 2018;13(7):e0197898.
    doi: 10.1371/journal.pone.0197898pmc: PMC6040684pubmed: 29995876google scholar: lookup
  44. Lindsey AA, Barton JDJ, Miles SR. Field Efficiencies of Forest Sampling Methods.. Ecology 1958;39(3):428–44.
  45. Pollock J. Behavioural ecology and body condition changes in New Forest ponies.. Scientific Publications of the RSPCA 1980;6:1–118.
  46. R Development Core Team. R: A Language and Environment for Statistical Computing.. 2.13.1 ed Vienna, Austria: R Foundation for Statistical Computing; 2011.
  47. Pinheiro JCP, Bates DM. Mixed-effects models in S and S-PLUS.. Berlin: Springer; 2000. xvi, 528 p.
  48. Bates D, Maechler M, Bolker B, Walker S, Bojesen Christensen RH, Singmann H. Linear Mixed-Effects Models using 'Eigen' and S4.. CRAN 2018;Package ‘lme4’:1–115.
  49. Burnham KP, Anderson DR. Model selection and multimodel inference: A practical information-theoretic approach.. Second ed New York, NY, USA: Springer-Verlag; 2002.
  50. Therneau T. survival: A Package for Survival Analysis in S.. R package version 2.36–12. URL http://CRANR-projectorg/package=survival. 2012.
  51. Klein JP, Moeschberger ML. Survival Analysis: Techniques for Censored and Truncated Data.. New York, NY: Springer; 2003.
  52. . Guidelines for the treatment of animals in behavioural research and teaching.. Animal Behaviour 2018;135:I–X.
  53. Stanton MA, Mann J. Early social networks predict survival in wild bottlenose dolphins.. PLoS One 2012;7(10):e47508.
    doi: 10.1371/journal.pone.0047508pmc: PMC3471847pubmed: 23077627google scholar: lookup
  54. Nuñez CMV, Adelman JS, Rubenstein DI. Sociality increases juvenile survival after a catastrophic event in the feral horse (Equus caballus).. Behavioral Ecology 2015;26(1):138–47.
  55. Lingle S, Wyman MT, Kotrba R, Teichroeb LJ, Romanow CA. What makes a cry a cry? A review of infant distress vocalizations.. Current Zoology 2015;58(5):698–726.
  56. Briefer EF. Vocal expression of emotions in mammals: Mechanisms of production and evidence.. Journal of Zoology 2012;288(1):1–20.
  57. Briefer EF, Maigrot AL, Mandel R, Freymond SB, Bachmann I, Hillmann E. Segregation of information about emotional arousal and valence in horse whinnies.. Sci Rep 2015 Apr 21;4:9989.
    pmc: PMC4404681pubmed: 25897781doi: 10.1038/srep09989google scholar: lookup
  58. Maigrot AL, Hillmann E, Anne C, Briefer EF. Vocal expression of emotional valence in Przewalski's horses (Equus przewalskii).. Sci Rep 2017 Aug 18;7(1):8779.
    doi: 10.1038/s41598-017-09437-1pmc: PMC5562828pubmed: 28821880google scholar: lookup
  59. Lee PC, Moss CJ. Early maternal investment in male and female African elephant calves.. Behavioral Ecology and Sociobiology 1986;18(5):353–61.
  60. Nowak R, Porter RH, Lévy F, Orgeur P, Schaal B. Role of mother-young interactions in the survival of offspring in domestic mammals.. Rev Reprod 2000 Sep;5(3):153-63.
    doi: 10.1530/ror.0.0050153pubmed: 11006165google scholar: lookup
  61. Sayigh LS, Tyack PL, Wells RS, Scott MD. Signature whistles of free-ranging bottlenose dolphins Tursiops truncatus: Stability and mother-offspring comparisons.. Behavioral Ecology and Sociobiology 1990;26(4):247–60.
  62. Tomasello M, George BL, Kruger AC, Jeffrey M, Farrar, Evans A. The development of gestural communication in young chimpanzees.. Journal of Human Evolution 1985;14(2):175–86.
  63. Hamel JA, Cocroft RB. Negative feedback from maternal signals reduces false alarms by collectively signalling offspring.. Proc Biol Sci 2012 Sep 22;279(1743):3820-6.
    pmc: PMC3415924pubmed: 22787019doi: 10.1098/rspb.2012.1181google scholar: lookup
  64. Théoret-Gosselin R, Hamel S, Côté SD. The role of maternal behavior and offspring development in the survival of mountain goat kids.. Oecologia 2015 May;178(1):175-86.
    doi: 10.1007/s00442-014-3198-xpubmed: 25556294google scholar: lookup
  65. Larsen KW, Boutin S. Movements, survival, and settlement of red squirrel (Tamiasciurus hudsonicus) offspring.. Ecology 1994;75(1):214–23.

Citations

This article has been cited 4 times.
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