• Abstract

    In several species of mammals, allonursing is a common practice in which maternal care of nonfilial offspring is provided. Allonursing benefits both mothers and young people. Although this phenomenon is not frequently observed in ungulates, different authors have reported this behavior in water buffaloes (Bubalus bubalis). However, it is still unclear why animals engage in alloparenting and, particularly, allosuckling when milk production has a high energetic cost. To explain this, several hypotheses have been proposed to understand the benefits that can be represented for the dam (e.g., improve maternal skill or milk evacuation) and the reasons that may motivate young people to be fed from nonfilial mothers (e.g., compensate for deficient milk intake). This review aims to discuss allomaternal care in Bubalus bubalis to understand how allonursing helps both females and offspring. Studies concerning allonursing are still limited in water buffalo, but current research suggests that some of the hypotheses to explain this strategy are parenting and compensation, among others.

  • References

    1. Bienboire-Frosini C, Marcet-Rius M, Orihuela A, Domínguez-Oliva A, Mora-Medina P, Olmos-Hernández A, et al (2023) Mother–Young Bonding: Neurobiological Aspects and Maternal Biochemical Signaling in Altricial Domesticated Mammals. Animals 13:532. https://doi.org/10.3390/ani13030532
    2. Brandlová K, Bartoš L, Haberová T (2013) Camel Calves as Opportunistic Milk Thefts? The First Description of Allosuckling in Domestic Bactrian Camel (Camelus bactrianus). PLoS ONE 8:e53052. https://doi.org/10.1371/journal.pone.0053052
    3. Briga M, Pen I, Wright J (2012) Care for kin: within-group relatedness and allomaternal care are positively correlated and conserved throughout the mammalian phylogeny. Biology Letters 8:533–536. https://doi.org/10.1098/rsbl.2012.0159
    4. Broad K, Curley J, Keverne E (2006) Mother–infant bonding and the evolution of mammalian social relationships. Philosophical Transactions of the Royal Society B: Biological Sciences 361:2199. https://doi.org/10.1098/RSTB.2006.1940
    5. Cameron EZ, Setsaas TH, Linklater WL (2009) Social bonds between unrelated females increase reproductive success in feral horses. Proceedings of the National Academy of Sciences 106:13850–13853. https://doi.org/10.1073/pnas.0900639106
    6. Cant MA (2012) Cooperative breeding systems. In: Royle NJ, Smiseth PT, Kölliker M (eds) The Evolution of Parental Care. Oxford University Press, Oxford, England, pp 206–225
    7. Carter CS, Altemus M (1977) Integrative functions of lactational hormones in social behavior and stress management. Ann. N. Y. Academic Science 807: 164–174, doi:10.1111/j.1749-6632.1997.tb51918.x.
    8. Cerrito P (2022) A milk-sharing economy allows placental mammals to overcome their metabolic limits. 119:1–8. https://doi.org/10.1073/pnas.2114674119/-/DCSupplemental.Published
    9. Clutton-Brock TH (2006) Cooperative breeding in mammals. In: Kappeler PM, Schaik CP (eds) Cooperation in Primates and Humans. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 173–190
    10. Dalto AC, Bandarra PM, Pavarini SP, et al (2012) Clinical and pathological insights into Johne′s disease in buffaloes. Tropical Animal Health and Production 44:1899–1904. https://doi.org/10.1007/S11250-012-0154-9
    11. de Oliveira Terceiro FE, Burkart JM (2019) Cooperative Breeding. In: Vonk J, Shackelford T (eds) Encyclopedia of Animal Cognition and Behavior,.Springer, Cham, Switzerland, pp 1–6
    12. Dubey P, Singh RR, Choudhary SS, Verma KK, Kumar A, Gamit PM, et al (2018) Post parturient neonatal behaviour and their relationship with maternal behaviour score, parity and sex in surti buffaloes. Journal of Applied Animal Research 46:6533. https://doi.org/10.1080/09712119.2017.1306533
    13. El-Regalaty H, Aboul-Ela H (2014) Non-genetic factors affecting incidence of abortion, stillbirth and post-natal mortality of Egyptian buffaloes. Journal of Animal and Poultry Production 5:313–324. https://doi.org/10.21608/jappmu.2014.70513
    14. Engelhardt SC, Weladji RB, Holand Ø, de Rioja CM, Ehmann RK, Nieminen M (2014) Allosuckling in reindeer (Rangifer tarandus): Milk-theft, mismothering or kin selection? Behavioural Processes 107:133–141. https://doi.org/10.1016/J.BEPROC.2014.08.013
    15. Engelhardt SC, Weladji RB, Holand Ø, Nieminen M (2016a) Allonursing in reindeer, Rangifer tarandus : a test of the kin-selection hypothesis. Journal of Mammalogy 97:689–700. https://doi.org/10.1093/JMAMMAL/GYW027
    16. Engelhardt SC, Weladji RB, Holand Ø, Røed KH, Nieminen M (2015) Evidence of Reciprocal Allonursing in Reindeer, Rangifer tarandus. Ethology 121:245–259. https://doi.org/10.1111/ETH.12334
    17. Engelhardt SC, Weladji RB, Holand Ø, Nieminen M (2016b) Allosuckling in reindeer (Rangifer tarandus): A test of the improved nutrition and compensation hypotheses. Mammalian Biology 81:. https://doi.org/10.1016/j.mambio.2015.10.003
    18. Fischer S, Pujol NT, Bolton R, Hurst JL, Stockley P (2018) Communal breeding affects offspring behaviours associated with a competitive social environment. Scientific Reports 8:16850. https://doi.org/10.1038/s41598-018-35089-w
    19. García-Ruiz I, Quiñones A, Taborsky M (2022) The evolution of cooperative breeding by direct and indirect fitness effects. Science Advances 8:7853. https://doi.org/10.1126/sciadv.abl7853
    20. Ghazanfar AA, Takahashi DY (2017) The Evo-Devo of Vocal Communication: Insights From Marmoset Monkeys. In: Kaas JH (ed) Evolution of Nervous Systems, 2nd edn. Academic Press, USA, pp 317–324
    21. Glasper ER, Kenkel WM, Bick J, Rilling JK (2019) More than just mothers: The neurobiological and neuroendocrine underpinnings of allomaternal caregiving. Frontiers in Neuroendocrinology 53:100741. https://doi.org/10.1016/j.yfrne.2019.02.005
    22. Gloneková M, Brandlová K, Pluháček J (2016) Stealing milk by young and reciprocal mothers: high incidence of allonursing in giraffes, Giraffa camelopardalis. Animal Behaviour 113:113–123. https://doi.org/10.1016/J.ANBEHAV.2015.11.026
    23. Gloneková M, Brandlová K, Pluháček J (2021) Further behavioural parameters support reciprocity and milk theft as explanations for giraffe allonursing. Scientific Reports 2021 11:1 11:1–9. https://doi.org/10.1038/s41598-021-86499-2
    24. Hadad E, Balaban A, Yosef R (2023) Alloparenting by Helpers in Striped Hyena (Hyaena hyaena). Animals 13:1914. https://doi.org/10.3390/ani13121914
    25. Hossein-Zadeh NG, Madad M, Shadparvar A, Kianzad D (2012) An observational analysis of secondary sex ratio, stillbirth and birth weight in Iranian Buffaloes (Bubalus bubalis). Journal of Agricultural Science and Technology 14:1477–1484
    26. Jennions MD, Macdonald DW (1994) Cooperative breeding in mammals. 9:89–93. https://doi.org/10.1016/0169-5347(94)90202-X
    27. Jo Manning C, Dewsbury DA, Wakeland EK, Potts WK (1995) Communal nesting and communal nursing in house mice, Mus musculus domesticus. Animal Behaviour 50:741–751. https://doi.org/10.1016/0003-3472(95)80134-0
    28. Kamikawa A, Seko J (2020) Physiological and pharmacological evaluation of oxytocin-induced milk ejection in mice. Experimental Animals 69:345–353. https://doi.org/10.1538/expanim.19-0126
    29. Kathe K, Yadav B. (2010) Incidence of mastitis in Sahiwal cattle and Murrah buffaloes of a closed organized herd. Indian Jounal of Animal Sciences 80:467–469
    30. Kenkel WM, Perkeybile AM, Carter CS (2017) The neurobiological causes and effects of alloparenting. Developmental Neurobiology 77:214–232. https://doi.org/10.1002/dneu.22465
    31. Kokko H, Johnstone RA, Clutton-Brock TH (2001) The evolution of cooperative breeding through group augmentation. Proceedings of the Royal Society B: Biological Sciences 268:1349. https://doi.org/10.1098/rspb.2000.1349
    32. Lee PC (1987) Allomothering among African elephants. Animal Behaviour 35:278–291. https://doi.org/10.1016/S0003-3472(87)80234-8
    33. Lent PC (1974) Mother-infant relationships in ungulates. In: Geist V, Walther F (eds) The behaviour of ungulates and its relation to management. Unwin Brothers Limited, Morges, Switzerland, pp 14–55
    34. Leung ES, Vergara V, Barrett-Lennard LG (2010) Allonursing in captive belugas (Delphinapterus leucas). Zoo Biology 29:633–637. https://doi.org/10.1002/zoo.20295
    35. Lewandrowski N, Hurnik J (1983) Nursing and cross-nursing behavior of beef cattle in cofinement. Canadian Journal of Animal Science 63:849–853
    36. Lezama-García K, Mariti C, Mota-Rojas D, Martínez-Burnes J, Barrios-García H, Gazzano A (2019) Maternal behaviour in domestic dogs. International Journal of Veterinary Science and Medicine 7:20–30. https://doi.org/10.1080/23144599.2019.1641899
    37. Lightman SL (1992) Alterations in hypothalamic-pituitary responsiveness during lactation. Ann. N. Y. Academic Science 652: 340–346, doi:10.1111/j.1749-6632.1992.tb34365.x.
    38. Lotito D, Pacifico E, Matuozzo S, Musco N, Iommelli P, Tudisco R, et al (2023) Colostrum management for buffalo calves : A review. 1:1–12. https://doi.org/10.20944/preprints202302.0248.v1
    39. Lupoli B, Johansson B, Uvnäs-Moberg K, Svennersten-Sjaunja K (2001) Effect of suckling on the release of oxytocin, prolactin, cortisol, gastrin, cholecystokinin, somatostatin and insulin in dairy cows and their calves. Journal of Dairy Research 68:175–187. https://doi.org/10.1017/S0022029901004721
    40. Maniscalco JM, Harris KR, Atkinson S, Parker P (2007) Alloparenting in Steller sea lions (Eumetopias jubatus): Correlations with misdirected care and other observations. Journal of Ethology 25:1–4. https://doi.org/10.1007/s10164-006-0001-4
    41. Miková K, Sovják R (2005) A review: Possibilities of allosuckling occurrence in camels (Camelus bactrianus). Agricultura Tropica et Subtropica 38:91–94
    42. Moen AN (1978) Seasonal Changes in Heart Rates, Activity, Metabolism, and Forage Intake of White-Tailed Deer. The Journal of Wildlife Management 42:763. https://doi.org/10.2307/3800763
    43. Monticelli PF, Tokumaru RS, Ades C (2018) Allosuckling in a captive group of wild cavies Cavia aperea. Mammalia 82:355–359. https://doi.org/10.1515/MAMMALIA-2016-0060
    44. Mora-Medina P, Napolitano F, Mota-Rojas D, Berdugo-Gutiérrez J, Ruiz-Buitrago J, Guerrero-Legarreta I (2018a) Imprinting, sucking and allosucking behaviors in buffalo calves. Journal of Buffalo Science 7:49–57.
    45. Mora-Medina P, Orihuela-Trujillo A, Roldan-Santiago P, Arch-Tirado E, Vázquez-Cruz C, Mota-Rojas D (2018b) Metabolic changes during brief periods of ewe–lamb separation at different ages. Animal Production Science 58:1297. https://doi.org/10.1071/AN16221
    46. Mota-Rojas D, Bragaglio A, Braghieri A, Napolitano F, Domínguez-Oliva A, Mora-Medina P, et al (2022a) Dairy Buffalo Behavior: Calving, Imprinting and Allosuckling. Animals 12:2899. https://doi.org/10.3390/ani12212899
    47. Mota-Rojas D, Marcet-Rius M, Domínguez-Oliva A, Martínez-Burnes J, Lezama-García K, Hernández-Ávalos I, et al (2023) The Role of Oxytocin in Domestic Animal’s Maternal Care: Parturition, Bonding, and Lactation. Animals 13:1207. https://doi.org/10.3390/ani13071207
    48. Mota-Rojas D, Marcet-Rius M, Freitas-de-Melo A, Muns R, Mora-Medina P, Domínguez-Oliva A, et al (2021) Allonursing in Wild and Farm Animals: Biological and Physiological Foundations and Explanatory Hypotheses. Animals 11:3092. https://doi.org/10.3390/ani11113092
    49. Mota-Rojas D, Marcet-Rius M, Freitas-de-Melo A, Strappini AC, Muns R, Domínguez-Oliva A, et al (2022b) Comportamiento de aloamamantamiento y sus posibles hipótesis: aspectos biológicos. In: Napolitano F, Mota-Rojas D, Orihuela A, et al. (eds) El búfalo de agua en las Américas. Comportamiento y productividad, 4th edn. B.M. Editores, Mexico City, Mexico, pp 596–625
    50. Mota-Rojas D, Martínez-Burnes J, Napolitano F, Domínguez-Muñoz M, Guerrero-Legarreta I, Mora-Medina P, et al (2020) Dystocia: factors affecting parturition in domestic animals. CABI Reviews 2020:1–16. https://doi.org/10.1079/PAVSNNR202015013
    51. Mota-Rojas D, Rosa G de, Mora-Medina P, et al (2019) Dairy buffalo behaviour and welfare from calving to milking. CABI Reviews 14:1–9. https://doi.org/10.1079/PAVSNNR201914035
    52. Mota-Rojas D, Whittaker AL, Domínguez-Oliva A, Strappini AC, Álvarez-Macías A, Grandin T et al (2024a). Tactile, auditory, and visual stimulation as sensory enrichment for dairy cattle. Animals 14: 1265. https://doi.org/10.3390/ani14091265
    53. Mota-Rojas D, Whittaker AL, Strappini AC, Orihuela A, Domínguez-Oliva A, Grandin T et al (2024b). Human animal relationships in Bos indicus cattle breeds addressed from a Five Domains welfare framework. Frontiers Veterinary Science 11:1456120. https://doi.org/10.3389/fvets.2024.1456120
    54. Mota-Rojas D, Bienboire-Frosini C, Orihuela A, Domínguez-Oliva A, Villanueva García D, Grandin T et al (2024c). Mother–Offspring Bonding after Calving in Water Buffalo and Other Ruminants: Sensory Pathways and Neuroendocrine Aspects. Animals 14: 2696. https://doi.org/10.3390/ani14182696
    55. Murphey RM, Paranhos da Costa MJR, Da Silva RG, de Souza RC (1995) Allonursing in river buffalo, Bubalus bubalis: nepotism, incompetence, or thievery? Animal Behaviour 49:1611–1616. https://doi.org/10.1016/0003-3472(95)90083-7
    56. Murphey RM, Paranhos da Costa MJR, de Souza Lima LO, de Moura Duarte FA (1991) Communal suckling in water buffalo (Bubalus bubalis). Applied Animal Behaviour Science 28:341–352. https://doi.org/10.1016/0168-1591(91)90166-U
    57. Napolitano F, Braghieri A, Bragaglio A, Rodríguez-González D, Mora-Medina P, Ghezzi M D, et al (2022a) Neurophysiology of Milk Ejection and Prestimulation in Dairy Buffaloes. Animals 12:2649. https://doi.org/10.3390/ani12192649
    58. Napolitano F, Mota-Rojas D, Braghieri A, Orihuela A, Álvarez-Macías A, Rodríguez D, et al (2022b) Asistencia al parto y eficacia del ordeño en la búfala de agua, aspectos etológicos y neuroanatómicos. Sociedades Rurales, Producción y Medio Ambiente 22:85–123
    59. Numan M (2015) Parental Behavior. In: Numan M (ed) Neurobiology of Social Behavior. Academic Press, London, UK, pp 165–234.
    60. Olazábal DE, Young LJ (2006a) Oxytocin receptors in the nucleus accumbens facilitate “spontaneous” maternal behavior in adult female prairie voles. Neuroscience 141:559–568. https://doi.org/10.1016/j.neuroscience.2006.04.017
    61. Olazábal DE, Young LJ (2006b) Species and individual differences in juvenile female alloparental care are associated with oxytocin receptor density in the striatum and the lateral septum. Hormones and Behavior 49:681–687. https://doi.org/10.1016/j.yhbeh.2005.12.010
    62. Oliveira ADFM, Quirino CR, Bastos R (2017) Effect of nursing behaviour, sex of the calf, and parity order on milk production of buffaloes. Revista Colombiana de Ciencias Pecuarias 30:30–38. https://doi.org/10.17533/udea.rccp.v30n1a04
    63. Olléová M, Pluháček J, King SRB (2012) Effect of social system on allosuckling and adoption in zebras. Journal of Zoology 288:127–134. https://doi.org/10.1111/J.1469-7998.2012.00930.X
    64. Orihuela A, Pérez-Torres LI, Ungerfeld R (2021) Evidence of cooperative calves’ care and providers’ characteristics in zebu cattle (Bos indicus) raised under extensive conditions. Tropical Animal Health and Production 53:143. https://doi.org/10.1007/s11250-020-02451-y
    65. Osman K., El-Enbaawy MI, Ezzeldeen N., Hussein HM. (2009) Mastitis in dairy buffalo and cattle in Egypt due to Clostridium perfringens: prevalence, incidence, risk factors and cost. Rev Sci Tech Off iIt Epiz 28:975–986
    66. Packer C, Lewis S, Pusey A (1992) A comparative analysis of non-offspring nursing. Animal Behaviour 43:265–281. https://doi.org/10.1016/S0003-3472(05)80222-2
    67. Paranhos da Costa MJR, Albuquerque LG, Eler JP, Augusto II de Vasconcelos Silva J (2006) Suckling behaviour of Nelore, Gir and Caracu calves and their crosses. Applied Animal Behaviour Science 101:276–287. https://doi.org/10.1016/j.applanim.2006.02.006
    68. Paranhos Da Costa MJR, Andriolo A, Simplício De Oliveira JF, Schmidek WR (2000) Suckling and allosuckling in river buffalo calves and its relation with weight gain. Applied Animal Behaviour Science 66:1–10. https://doi.org/10.1016/S0168-1591(99)00083-0
    69. Poindron P (2005) Mechanisms of activation of maternal behaviour in mammals. Reproduction Nutrition Development 45:341–351. https://doi.org/10.1051/rnd:2005025
    70. Pusey AE, Packer C (1994) Non-offspring mursing in social carnivores: minimizing the cost. Bheavioral Ecology 5:362–374
    71. Roulin A (2002) Why do lactating females nurse alien offspring? A review of hypotheses and empirical evidence. Animal Behaviour 63:201–208. https://doi.org/10.1006/ANBE.2001.1895
    72. Roulin A, Heeb P (1999) The immunological function of allosuckling. Ecology Letters 2:319–324. https://doi.org/10.1046/J.1461-0248.1999.00091.X
    73. Silveira PA, Spoon RA, Ryan DP, Williams GL (1993) Evidence for Maternal Behavior as a Requisite Link in Suckling-Mediated Anovulation in Cows1. Biology of Reproduction 49:1338–1346. https://doi.org/10.1095/biolreprod49.6.1338
    74. Singh NP, Kamboj ML (2023) Influence of Maternal Contact on Hormonal, Growth, and Behavioral Responses of Murrah Buffalo Calves in Winter. International Journal of Environment and Climate Change 13:1635–1645. https://doi.org/10.9734/ijecc/2023/v13i113318
    75. Špinka M, Illmann G (1992) Suckling behaviour of young dairy calves with their own and alien mothers. Applied Animal Behaviour Science 33:165–173. https://doi.org/10.1016/S0168-1591(05)80005-X
    76. Stábile F (2013) Aloamamantamiento en Arctocephalus australis en Isla de Lobos (Uruguay): Estrategia individual de las crías? Universidad de la República de Uruguay
    77. Stead S, Mucha S, Bădescu I (2019) Alloparental Care. In: Vonk J, Shackelford T (eds) Encyclopedia of Animal Cognition and Behavior. Springer, Cham, Switzerland, pp 1–7
    78. Tecot SR, Baden AL, Romine N, Kamilar JM (2013) Reproductive Strategies and Infant Care in the Malagasy Primates. In: Clancy KB., Hinde K, Rutherford JN (eds) Building Babies. Springer New York, New York, NY, USA, pp 321–359
    79. Teja A, Jeyakumar S, Rao KA, et al (2023) Pre- and peri parturient behaviour as an indicator of onset of the calving process in Murrah buffalo (Bubalus bubalis). Applied Animal Behaviour Science 263:105936. https://doi.org/10.1016/j.applanim.2023.105936
    80. Thompson K V, Baker AJ, Baker AM (2010) Parental care and behavioral development in captive mammals. In: Kleiman DG, Thompson K V, Baer CK (eds) Wild mammals in captivity. Principles and techniques for zoo management, 2nd editio. The University of Chicago Press, USA, pp 367–385
    81. Trivers RL (1971) The Evolution of Reciprocal Altruism. The Quarterly Review of Biology 46:. https://doi.org/10.1086/406755
    82. Val-Laillet D, Nowak R (2006) Socio-spatial criteria are important for the establishment of maternal preference in lambs. Applied Animal Behaviour Science 96:269–280. https://doi.org/10.1016/J.APPLANIM.2005.07.010
    83. Víchová J, Bartoš L (2005) Allosuckling in cattle: Gain or compensation? 94:223–235. https://doi.org/10.1016/j.applanim.2005.02.015
    84. Wilkinson GS (1992) Communal nursing in the evening bat, Nycticeius humeralis. Behavioral Ecology and Sociobiology 1992 31:4 31:225–235. https://doi.org/10.1007/BF00171677
    85. Yamaguchi S, Aoki N, Kitajima T, Iikubo E, Katagiri S, Matsushima T, et al (2012) Thyroid hormone determines the start of the sensitive period of imprinting and primes later learning. Nature Communications 3:1081. https://doi.org/10.1038/ncomms2088
    86. Zapata B, Correa L, Soto-Gamboa M, Latorre E, González BA, Ebensperger LA (2010) Allosuckling allows growing offspring to compensate for insufficient maternal milk in farmed guanacos (Lama guanicoe). Applied Animal Behaviour Science 122:119–126. https://doi.org/10.1016/J.APPLANIM.2009.12.004
    87. Zapata B, Gaete G, Correa LA, González BA, Ebensperger LA (2009a) A case of allosuckling in wild guanacos (Lama guanicoe). Journal of Ethology 27:295–297. https://doi.org/10.1007/s10164-008-0127-7
    88. Zapata B, González BA, Ebensperger LA (2009b) Allonursing in Captive Guanacos, Lama guanicoe: Milk Theft or Misdirected Parental Care? Ethology 115:731–737. https://doi.org/10.1111/J.1439-0310.2009.01660.X

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Orihuela, A., Bienboire-Frosini , C., Chay-Canul , A., Álvarez-Macías , A., Marcet-Rius , M., Domínguez-Oliva , A., Mora-Medina, P., Olmos-Hernández, A., Napolitano, F., García-Herrera , R., & Mota-Rojas, D. (2024). Allonursing in water buffalo: Cooperative maternal behavior in domestic <em>Bovidae</em>. Journal of Animal Behaviour and Biometeorology, 12(3), 2024023. https://doi.org/10.31893/jabb.2024023
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