Nursing Behaviour in Alpacas: Parallels in the Andes and Central Europe, and a Rare Allonursing Occurrence
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
IGA-20243112
Internal grant agency (IGA) FTZ CZU, Prague
IGA-20243107
Internal grant agency (IGA) FTZ CZU, Prague
N/A
Foundation of Josef, Marie and Zdenka Hlavka
PubMed
40218310
PubMed Central
PMC11987768
DOI
10.3390/ani15070916
PII: ani15070916
Knihovny.cz E-zdroje
- Klíčová slova
- Vicugna pacos, allosuckling, maternal behaviour, nursing duration, nursing of crias,
- Publikační typ
- časopisecké články MeSH
Understanding maternal behaviour is essential for good animal husbandry; yet, little scientific information currently exists regarding nursing behaviour of alpacas (Vicugna pacos). Moreover, allonursing (the nursing of non-filial offspring) has only been documented in captive non-domesticated guanacos. This study aimed to (1) describe the nursing behaviour of alpacas within traditional husbandry systems in their place of origin, and in foreign conditions, and to (2) investigate the occurrence of allonursing in alpacas. A total of 1899 nursing bouts were observed in the Andes and Central Europe. Additionally, 102 Andean farmers were asked if they observed allonursing in their herds. Nursing behaviour was similar at both locations, with most of the nursing bouts initiated by crias and terminated by dams. However, several significant differences between localities were noted, such as the less frequent sniffing of crias by Andean dams. Crias' age and sex did not affect the percentage of nursing bouts initiated or terminated by the dams. Rare cases of allonursing were recorded in Central Europe (n = 5), and 18.6% of surveyed Andean farmers reported allonursing in their herds. This study provides insight into alpaca nursing and allonursing behaviour, which may contribute towards their management both in their place of origin and farther.
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Miranda-de la Lama G.C., Villarroel M. Behavioural biology of South American domestic camelids: An overview from a welfare perspective. Small Rumin. Res. 2023;220:106918. doi: 10.1016/j.smallrumres.2023.106918. DOI
Germana Cavero C., Chaquilla O., Santos G., Ferrari M., Krusich C., Kindgard F.M. Estudio Socioeconómico de los Pastores Andinos de Perú, Ecuador, Bolivia y Argentina. El Alva; Arequipa, Peru: 2016.
FAOSTAT: Crops and Livestock Products. [(accessed on 4 June 2023)]. Available online: https://www.fao.org/faostat/en/#data/QCL.
Gauly M., Egen W., Trah M. Zur Haltung von Neuweltkameliden in Mitteleuropa. Tierarztl. Umsch. 1997;52:343–350.
Davis R., Keeble E., Wright A., Morgan K.L. South American camelids in the United Kingdom: Population statistics, mortality rates and causes of death. Vet. Rec. 1998;142:162–166. doi: 10.1136/vr.142.7.162. PubMed DOI
Neubert S., von Altrock A., Wendt M., Wagener M.G. Llama and Alpaca Management in Germany—Results of an Online Survey among Owners on Farm Structure, Health Problems and Self-Reflection. Animals. 2021;11:102. doi: 10.3390/ani11010102. PubMed DOI PMC
Middleton A., Blackie N., Crilly J.P., Reilly B. Survey of current UK alpaca husbandry practices: Vaccination, treatment and supplementation. Vet. Rec. 2023;194:e3602. doi: 10.1002/vetr.3602. PubMed DOI
Chaplin S.J., Gretgrix L. Effect of housing conditions on activity and lying behaviour of horses. Animal. 2010;4:792–795. doi: 10.1017/S1751731109991704. PubMed DOI
Leliveld L.M., Riva E., Mattachini G., Finzi A., Lovarelli D., Provolo G. Dairy cow behavior is affected by period, time of day and housing. Animals. 2022;12:512. doi: 10.3390/ani12040512. PubMed DOI PMC
Pouillon C., Erhard G., Gauly M. Suckling Behaviour of Llama (Lama glama). Progress in South American Camelids Research. Dtsch. Tierarztl. Wochenschr. 2001;110:412–416. PubMed
Vaarst M., Lund V., Roderick S., Lockeretz W., editors. Animal Health and Welfare in Organic Agriculture. CABI Publishing; Wallingford, UK: 2004. pp. 73–91.
Ekesbo I., Gunnarsson S. Farm animal Behaviour: Characteristics for Assessment of Health and Welfare. 2nd ed. CABI Publishing; Wallingford, UK: 2018. pp. 1–156.
Lévy F., Keller M., Poindron P. Olfactory regulation of maternal behavior in mammals. Horm. Behav. 2004;46:284–302. PubMed
Corona R., Lévy F. Chemical Olfactory Signals and Parenthood in Mammals. Horm. Behav. 2015;68:77–90. PubMed
Torriani M.V., Vannoni E., McElligott A.G. Mother-young recognition in an ungulate hider species: A unidirectional process. Am. Nat. 2006;168:412–420. doi: 10.1086/506971. PubMed DOI
Zapata B., Correa L., Soto-Gamboa M., Latorre E., González B.A., Ebensperger L.A. Allosuckling allows growing offspring to compensate for insufficient maternal milk in farmed guanacos (Lama guanicoe) Appl. Anim. Behav. Sci. 2010;122:119–126. doi: 10.1016/j.applanim.2009.12.004. DOI
Hammadi I., Chniter M., Atigui M., Brahmi M., Seddik M.M., Salem W.B., Hammadi M. Dam parity and calf sex affect maternal and neonatal behaviors during the first week postpartum in stabled Maghrebi dairy camels. Animal. 2021;15:100149. doi: 10.1016/j.animal.2020.100149. PubMed DOI
Zabek K., Swiatek M., Micinski J. Behavioural characteristics of female alpacas and their crias during early rearing. Anim. Sci. Genet. 2024;20:37–45. doi: 10.5604/01.3001.0054.8447. DOI
Okorie A.U., Sanda L.U. Rangeland and Grazing Reserve in Nigeria: Livestock Sub-Sector Review. Volume 2. FAO (Food and Agriculture Organization); Rome, Italy: 1922. pp. 2–15.
Martini M., Altomonte I., da Silva Sant’ana A.M., Del Plavignano G., Salari F. Gross, mineral and fatty acid composition of alpaca (Vicugna pacos) milk at 30 and 60 days of lactation. Small Rumin. Res. 2010;132:50–54. doi: 10.1016/j.smallrumres.2015.10.001. DOI
Tibary A., Johnson L.W., Pearson L.K., Rodriguez J.S. Lactation and neonatal care. In: Cebra C., Anderson D.E., Tibary A., Van Saun R.J., Johnson L.W., editors. Llama and Alpaca Care: Medicine, Surgery, Reproduction, Nutrition, and Herd Health. Elsevier Health Sciences; St. Louis, MO, USA: 2013. pp. 286–297.
Lidfors L.M., Jensen P., Algers B. Suckling in free-ranging beef cattle—Temporal patterning of suckling bouts and effects of age and sex. Ethology. 1994;98:321–332. doi: 10.1111/j.1439-0310.1994.tb01080.x. DOI
Ruiz-Miranda C.R., Thompson K.V., Callard M. Suckling behavior in domestic goats: Interaction between litter size and kid sex. Int. J. Comp. Psychol. 1998;11:93–111. doi: 10.46867/C4W89R. DOI
Hejcmanová P., Vymyslická P., Koláčková K., Antonínová M., Havlíková B., Stejskalová M., Policht R., Hejcman M. Suckling behavior of eland antelopes (Taurotragus spp.) under semi-captive and farm conditions. J. Ethol. 2011;29:161–168. doi: 10.1007/s10164-010-0241-1. DOI
von Keyserlingk M.A.G., Weary D.M. Maternal Behavior in Cattle. Horm. Behav. 2007;52:106–113. doi: 10.1016/j.yhbeh.2007.03.015. PubMed DOI
Barber J.A., Crowell-Davis S.L. Maternal behavior of Belgian (Equus caballus) mares. Appl. Anim. Behav. Sci. 1994;41:161–189. doi: 10.1016/0168-1591(94)90021-3. DOI
Crowell-Davis S.L. Nursing behaviour and maternal aggression among Welsh ponies (Equus caballus) Appl. Anim. Behav. Sci. 1985;14:11–25.
Brandlová K., Bartoš L., Haberová T. Camel Calves as Opportunistic Milk Thefts? The First Description of Allosuckling in Domestic Bactrian Camel (Camelus bactrianus) PLoS ONE. 2013;8:e53052. PubMed PMC
Komárková M., Bartošová J. Lateralized suckling in domestic horses (Equus caballus) Anim. Cogn. 2013;16:343–349. PubMed
Waltl B., Appleby M.C., Sölkner J. Effects of relatedness on the suckling behaviour of calves in a herd of beef cattle rearing twins. Appl. Anim. Behav. Sci. 1995;45:1–9.
Packer C., Lewis S., Pusey A. A comparative analysis of nonoffspring nursing. Anim. Behav. 1992;43:265–281.
Gloneková M., Brandlová K., Pluháček J. Stealing Milk by Young and Reciprocal Mothers: High Incidence of Allonursing in Giraffes, Giraffa camelopardalis. Anim. Behav. 2016;113:113–123.
Villagran M., De La Fuente L., Ungerfeld R. Pampas deer fawns (Ozotoceros bezoarticus, Linnaeus, 1758) feeding time budget during the first twelve weeks of life. North-West J. Zool. 2012;8:85–91.
Wronski T., Apio A., Wanker R., Plath M. Behavioural repertoire of the bushbuck (Tragelaphus scriptus): Agonistic interactions, mating behaviour and parent–offspring relations. J. Ethol. 2006;24:247–260.
Aba M.A., Bianchi C., Cavilla V. South American Camelids. In: Tynes V.V., editor. Behavior of Exotic Pets. Wiley-Blackwell; Hoboken, NJ, USA: 2010. pp. 157–165.
Gauthier D., Barrette C. Suckling and Weaning in Captive White-Tailed and Fallow Deer. Behaviour. 1985;94:128–149.
García y González E.G., Flores J.A., Delgadillo J.A., González-Quirino T., Fernández I.G., Terrazas A., Hernández H. Early nursing behaviour in ungulate mothers with hider offspring (Capra hircus): Correlations between milk yield and kid weight. Small Rumin. Res. 2017;151:59–65.
Kour H., Corbet N.J., Patison K.P., Swain D.L. Changes in the suckling behaviour of beef calves at 1 month and 4 months of age and effect on cow production variables. Appl. Anim. Behav. Sci. 2021;236:105219.
Hogan L., McGowan M.R., Johnston S.D., Lisle A.T., Schooley K. Suckling behaviour of beef calves during the first five days postpartum. Ruminants. 2022;2:321–340. doi: 10.3390/ruminants2030022. DOI
Gloneková M., Vymyslická P.J., Žáčková M., Brandlová K. Giraffe Nursing Behaviour Reflects Environmental Conditions. Behaviour. 2017;154:115–129.
Gloneková M., Brandlová K., Pluháček J. Further Behavioural Parameters Support Reciprocity and Milk Theft as Explanations for Giraffe Allonursing. Sci. Rep. 2021;11:7024. PubMed PMC
Gloneková M., Brandlová K., Pluháček J. Giraffe Males Have Longer Suckling Bouts than Females. J. Mammal. 2020;101:558–563.
Drábková J., Bartošová J., Bartoš L., Kotrba R., Pluháček J., Švecová L., Dušek A., Kott T. Sucking and allosucking duration in farmed red deer (Cervus elaphus) Appl. Anim. Behav. Sci. 2008;113:215–223.
Cameron E.Z., Linklater W.L., Stafford K.J., Minot E.O. Aging and improving reproductive success in horses: Declining residual reproductive value or just older and wiser? Behav. Ecol. Sociobiol. 2000;47:243–249.
Pluháček J., Bartošová J., Bartoš L. Suckling behavior in captive plains zebra (Equus burchellii): Sex differences in foal behavior. J. Anim. Sci. 2010;88:131–136. PubMed
Elmi A.A. Camel Husbandry and Management by Ceeldheer Pastoralists in Central Somalia. Agricultural Administration Unit, Overseas Development Institute; Mogadishu, Somalia: 1989.
Mota-Rojas D., Marcet-Rius M., Freitas-de-Melo A., Muns R., Mora-Medina P., Domínguez-Oliva A., Orihuela A. Allonursing in Wild and Farm Animals: Biological and Physiological Foundations and Explanatory Hypotheses. Animals. 2021;11:3092. doi: 10.3390/ani11113092. PubMed DOI PMC
Álvarez-Rodríguez J., Palacio J., Casasús I., Revilla R., Sanz A. Performance and nursing behaviour of beef cows with different types of calf management. Animal. 2009;3:871–878. doi: 10.1017/S175173110900408X. PubMed DOI
Thodberg K., Jensen K.H., Herskin M.S. Nursing behaviour, postpartum activity and reactivity in sows: Effects of farrowing environment, previous experience and temperament. Appl. Anim. Behav. Sci. 2002;77:53–76. doi: 10.1016/S0168-1591(02)00023-0. DOI
Vanheukelom V., Driessen B., Geers R. The effects of environmental enrichment on the behaviour of suckling piglets and lactating sows: A review. Livest. Sci. 2012;143:116–131. doi: 10.1016/j.livsci.2011.10.002. DOI
Therrien J.F., Côté S.D., Festa-Bianchet M., Ouellet J.P. Maternal care in white-tailed deer: Trade-off between maintenance and reproduction under food restriction. Anim. Behav. 2008;75:235–243. doi: 10.1016/j.anbehav.2007.04.030. DOI
González B.A., Palma R.E., Zapata B., Marín J.C. Taxonomic and biogeographical status of guanaco Lama guanicoe (Artiodactyla, Camelidae) Mamm. Rev. 2006;36:157–178. doi: 10.1111/j.1365-2907.2006.00084.x. DOI
Roulin A. Why do lactating females nurse alien offspring? A review of hypotheses and empirical evidence. Anim. Behav. 2002;63:201–208. doi: 10.1006/anbe.2001.1895. DOI
Landete-Castillejos T., Garcia A., Garde A., Gallego L. Milk intake and production curves and allosuckling in captive Iberian red deer, Cervus elaphus hispanicus. Anim. Behav. 2000;60:679–687. doi: 10.1006/anbe.2000.1515. PubMed DOI
Engelhardt S.C., Weladji R.B., Holand Ø., de Rioja C.M., Ehmann R.K., Nieminen M. Allosuckling in Reindeer (Rangifer tarandus): Milk-theft, Mismothering or Kin Selection? Behav. Process. 2014;107:133–141. doi: 10.1016/j.beproc.2014.08.013. PubMed DOI
MacLeod K.J., Lukas D. Revisiting non-offspring nursing: Allonursing evolves when the costs are low. Biol. Lett. 2014;10:20140378. doi: 10.1098/rsbl.2014.0378. DOI
Zapata B., Gonzalez B.A., Ebensperger L.A. Allonursing in captive guanacos, Lama guanicoe: Milk theft or misdirected parental care? Ethology. 2009;115:731–737. doi: 10.1111/j.1439-0310.2009.01660.x. DOI
Orihuela A., Bienboire-Frosini C., Chay-Canul A., Álvarez-Macías A., Marcet-Rius M., Domínguez-Oliva A., Mota-Rojas D. Allonursing in water buffalo: Cooperative maternal behavior in domestic Bovidae. J. Anim. Behav. Biometeorol. 2024;12:2024023. doi: 10.31893/jabb.2024023. DOI
Ekvall K. Effects of social organization, age and aggressive behaviour on allosuckling in wild fallow deer. Anim. Behav. 1998;56:695–703. doi: 10.1006/anbe.1998.0825. PubMed DOI
Pélabon C., Yoccoz N.G., Ropert-Coudert Y., Caron M., Peirera V. Suckling and Allosuckling in Captive Fallow Deer (Dama dama, Cervidae) Ethology. 1998;104:75–86.
Fiallos L., Herrera R.S., Velázquez R. Flora diversity in the Ecuadorian Páramo grassland ecosystem. Cuban J. Agric. Sci. 2016;49:399–405.
La Frenierre J., Mark B.G. Detecting Patterns of Climate Change at Volcán Chimborazo, Ecuador, by Integrating Instrumental Data, Public Observations, and Glacier Change Analysis. Ann. Am. Assoc. Geogr. 2017;107:979–997.
Montenegro B., Zuňiga S., Zeballos H. Climatología de la Reserva Nacional Salinas y Aguada Blanca, suroeste del Perú. In: Zeballos H., Zeballos H., Ochoa J.A., Lopez E., editors. Diversidad Biológica de la Reserva Nacional de Salinas y Aguada Blanca. Litho & Arte SAC; Lima, Peru: 2010. pp. 261–273.
Catorci A., Cesaretti S., Velasquez J.L., Malatesta L., Zeballos H. The interplay of land forms and disturbance intensity drive the floristic and functional changes in the dry Puna pastoral systems (southern Peruvian Andes) Plant Biosyst.-Int. J. Plant Biol. 2014;148:547–557.
Climate-Data. [(accessed on 14 February 2025)]. Available online: https://en.climate-data.org.
Šandlová K., Komárková M., Ceacero F. Daddy, daddy cool: Stallion–foal relationships in a socially-natural herd of Exmoor ponies. Anim. Cogn. 2020;23:781–793. PubMed
Pilarczyk B., Pilarczyk R., Sablik P. The impact of breeding and farming conditions on the welfare of alpacas (Vicugna pacos) Acta Sci. Pol. Zootech. 2023;22:3–8. doi: 10.21005/asp.2023.22.3.01. DOI
de Passillé A.M., Rabeyrin M., Rushen J. Associations between milk intake and activity in the first days of a calf’s life and later growth and health. Appl. Anim. Behav. Sci. 2016;175:2–7.
Mota-Rojas D., Marcet-Rius M., Domínguez-Oliva A., Martínez-Burnes J., Lezama-García K., Hernández-Ávalos I., Bienboire-Frosini C. The role of oxytocin in domestic animal’s maternal care: Parturition, bonding, and lactation. Animals. 2023;13:1207. doi: 10.3390/ani13071207. PubMed DOI PMC
Bryant F.C., Farfan R.D. Dry Season Forage Selection by Alpaca (Lama pacos) in Southern Peru. J. Range. Manag. 1984;37:330–333.
Bryant F.C., Florez A., Pfister J. Sheep and Alpaca Productivity on High Andean Rangelands in Peru. J. Anim. Sci. 1989;67:3087–3095. doi: 10.2527/jas1989.67113087x. DOI
Babiker W.I.A., El-Zubeir I.E.M. Impact of husbandry, stages of lactation and parity number on milk yield and chemical composition of dromedary camel milk. Emir. J. Food Agric. 2014;26:333–341. doi: 10.9755/ejfa.v26i4.17664. DOI
Weary D.M., Jasper J., Hötzel M.J. Understanding weaning distress. Appl. Anim. Behav. Sci. 2008;110:24–41. doi: 10.1016/j.applanim.2007.03.025. DOI
Abecia D.A., Canudo C., Palacios C., Canto F. Measuring lamb activity during lactation by actigraphy. Chronobiol. Int. 2022;39:1368–1380. PubMed
Stěhulová I., Špinka M., Šárová R., Máchová L., Kněz R., Firla P. Maternal behaviour in beef cows is individually consistent and sensitive to cow body condition, calf sex and weight. Appl. Anim. Behav. Sci. 2013;144:89–97. doi: 10.1016/j.applanim.2013.01.003. DOI
Marešová J., Kokošková T., Fedorova T. Husbandry and breeding practices of South American camelids in Ecuador and Peru, and the impact of country, gender, and farming experience thereon. Trop. Anim. Health Prod. :2025. submitted .
Coulon M., Baudoin C., Heyman Y., Deputte B.L. Cattle discriminate between familiar and unfamiliar conspecifics by using only head visual cues. Anim. Cogn. 2011;14:279–290. PubMed
Murphey R.M., Paranhos da Costa M.J.R., Gomes da Silva R., de Souza R. Allonursing in river buffalo, Bubalis bubalis: Nepotism, incompetence, or thievery? Anim. Behav. 1995;49:1611–1616.
Brown B.W. A review on reproduction in South American camelids. Anim. Reprod. Sci. 2000;58:169–195. doi: 10.1016/S0378-4320(99)00081-0. PubMed DOI
Saito M., Idani G. Suckling and Allosuckling Behavior in Wild Giraffe (Giraffa camelopardalis tippelskirchi) Mamm. Biol. 2018;93:1–4. doi: 10.1016/j.mambio.2018.07.005. DOI
Fedorova T. Ph.D. Thesis. Czech University of Life Sciences; Prague, Czech Republic: 2015. The Evaluation of Reproduction in Bactrian Camels (Camelus bactrianus) and the Possibilities of Using Non-invasive Methods for Detection of Heat and Pregnancy.
Kenyon P.R., Roca Fraga F.J., Blumer S., Thompson A.N. Triplet lambs and their dams—A review of current knowledge and management systems. N. Z. J. Agric. Res. 2019;62:399–437.
Bartoš L., Vaňková D., Hyánek J., Šiler J. Impact of allosucking on growth of farmed red deer calves (Cervus elaphus) Anim. Sci. 2001;72:493–500.
Víchová J., Bartoš L. Allosuckling in cattle: Gain or compensation? Appl. Anim. Behav. Sci. 2005;94:223–235.
Haberová T., Fedorov P. Umělý odchov velblouda dvouhrbého (Camelus bactrianus)—Hand-rearing of Bactrian camel (Camelus bactrianus) Gazella. 2012;39:67–75.