Further behavioural parameters support reciprocity and milk theft as explanations for giraffe allonursing
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
33782483
PubMed Central
PMC8007720
DOI
10.1038/s41598-021-86499-2
PII: 10.1038/s41598-021-86499-2
Knihovny.cz E-zdroje
- MeSH
- kojená zvířata * MeSH
- laktace * MeSH
- mléko * MeSH
- stravovací zvyklosti * MeSH
- žirafy fyziologie MeSH
- zvířata MeSH
- Check Tag
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Suckling of a non-filial calf, or allosuckling, is an extreme case of allomaternal care in mammals. There have been many hypotheses postulated in an attempt to explain this behaviour; however, the supporting evidence differs, together with the conclusions drawn from the investigated variables. Previously, suckling bout rejection was analysed, and the milk theft and reciprocity hypotheses were both determined as the most appropriate explanation of allosuckling in giraffe. In this study, seven hypotheses were tested using different behavioural parameters, namely suckling bout frequency, suckling bout duration, and time spent suckling. It is well-documented that these parameters are associated with various aspects in ungulate biology; for example, suckling rejection typically reflects milk intake and parent-offspring conflict, whereas the suckling bout duration and frequency is associated with social behaviours (affiliation, bonding, social stress). In total, 22 nursing females and 47 suckling calves were observed, in four Czech zoos during a five-year period. The correlation of the observed parameters between the reciprocal female-calf dyads was found to be in line with the reciprocity hypothesis. In addition, non-filial calves tried to steal the milk from non-maternal females, supporting the milk theft hypothesis. Thus, the results support both the reciprocity and milk-theft hypotheses as the most plausible explanation of allosuckling in giraffe, and illustrates the importance of using suckling bout duration and frequency, and the time spent suckling, as behavioural parameters that may aid in explaining the extremity of maternal investment, such as allosuckling.
Zobrazit více v PubMed
Rippeyoung PLF, Noonan MC. The economic costs of breastfeeding for women. Breastfeed Med. 2011;6(5):325–327. doi: 10.1089/bfm.2011.0083. PubMed DOI
Gloneková M, Vymyslická PJ, Žáčková M, Brandlová K. Giraffe nursing behaviour reflects environmental conditions. Behaviour. 2017;154:115–129. doi: 10.1163/1568539X-00003413. DOI
Hejcmanová P, Vymyslická P, Koláčková K, Antonínová M, Havlíková B, Stejskalová M, Policht R, Hejcman M. Suckling behaviour 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
Clutton-Brock TH. The Evolution of Parental Care. Princeton University Press; 1991.
Gittleman JL, Thompson SD. Energy allocation in mammalian reproduction. Am. Zool. 1988;28:863–875. doi: 10.1093/icb/28.3.863. DOI
Arnold LC, Habe M, Troxler J, Nowack J, Vetter SG. Rapid establishment of teat order and allonursing in wild boar (Sus scrofa) Ethology. 2019;125:940–948. doi: 10.1111/eth.12950. DOI
Pluháček J, Olléová M, Bartošová J, Bartoš L. Effect of ecological adaptation on suckling behaviour in three zebra species. Behaviour. 2012;149(13–14):1395–1411.
Pluháček J, Olléová M, Bartoš L, Bartošová J. Time spent suckling is affected by different social organization in three zebra species. J. Zool. 2014;292:10–17. doi: 10.1111/jzo.12077. DOI
Packer C, Lewis S, Pusey A. A comparative analysis of non-offspring nursing. Anim. Behav. 1992;43:265–281. doi: 10.1016/S0003-3472(05)80222-2. DOI
Gloneková M, Brandlová K, Pluháček J. Higher maternal care and tolerance in more experienced giraffe mothers. Acta Ethol. 2020;23:1–7. doi: 10.1007/s10211-019-00328-4. DOI
MacLeod K, Nielsen JF, Clutton-Brock TH. Factors predicting the frequency, likelihood and duration of allonursing in the cooperatively breeding meerkat. Anim. Behav. 2013;86:1059–1067. doi: 10.1016/j.anbehav.2013.09.012. DOI
König B. Cooperative care of young in mammals. Naturwissenschaften. 1997;84:489–497. PubMed
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
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. doi: 10.1017/S1357729800052012. DOI
Bartoš L, Vaňková D, Šiler J, Illmann G. Adoption, allonursing and allosucking in farmed red deer (Cervus elaphus) Anim. Sci. 2001;72:483–492. doi: 10.1017/S1357729800052000. DOI
Engelhardt SC, Weladji RB, Holand Ø, Nieminen M. Allosuckling in reindeer (Rangifer tarandus): A test of the improved nutrition and compensation hypotheses. Mammal. Biol. Z Säugetierkd. 2016;81(2):146–152. doi: 10.1016/j.mambio.2015.10.003. DOI
Víchová J, Bartoš L. Allosuckling in cattle: Gain or compensation? Appl. Anim. Behav. Sci. 2005;94:223–235. doi: 10.1016/j.applanim.2005.02.015. DOI
Engelhardt SC, Weladji RB, Holand Ø, de Rioja CM, Ehmann RK, 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
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. doi: 10.1016/j.anbehav.2015.11.026. DOI
Pluháček J, Bartošová J, Bartoš L. Suckling behavior in captive plains zebra (Equus burchellii): Sex differences in foal behavior. J. Anim. Sci. 2010;88(1):131–136. doi: 10.2527/jas.2009-1982. PubMed DOI
Gloneková M, Brandlová K, Pluháček J. Giraffe males have longer suckling bouts than females. J. Mammal. 2020;101(2):558–653. doi: 10.1093/jmammal/gyz201. DOI
Pluháček J, Bartošová J, Bartoš L. Further evidence for sex differences in suckling behaviour of captive plains zebra foals. Acta Ethol. 2011;14:91–95. doi: 10.1007/s10211-011-0091-z. DOI
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(1):215–223. doi: 10.1016/j.applanim.2007.10.009. DOI
Mendl M, Paul ES. Observation of nursing and sucking behaviour as an indicator of milk transfer and parental investment. Anim. Behav. 1989;37:513–515. doi: 10.1016/0003-3472(89)90100-0. DOI
Therrien JF, Cote SD, Festa-Bianchet M, Ouellet JP. Maternal care in white-tailed deer: Trade-off between maintenance and reproduction under food restriction. Anim. Behav. 2007;75:235–243. doi: 10.1016/j.anbehav.2007.04.030. DOI
Plesner Jensen S, Siefert L, Okori J, Clutton-Brock T. Age-related participation in allosuckling by nursing warthogs (Phacochoerus africanus) J. Zool. 1999;248:443–449. doi: 10.1111/j.1469-7998.1999.tb01044.x. DOI
Trivers RL. The evolution of reciprocal altruism. Q. Rev. Biol. 1971;46:35–57. doi: 10.1086/406755. DOI
Engelhardt SC, Weladji RB, Holand Ø, Røed KH, Nieminen M. Evidence of reciprocal allonursing in reindeer, Rangifer tarandus. Ethology. 2015;121(3):245–259. doi: 10.1111/eth.12334. DOI
Jones JD, Treanor JJ. Allonursing and cooperative birthing behavior in Yellowstone bison, Bison bison. Can. Field-Nat. 2008;122(2):171–172. doi: 10.22621/cfn.v122i2.579. DOI
Pusey AE, Packer C. Non-offspring nursing in social carnivores—Minimizing the costs. Behav. Ecol. 1994;5:362–374. doi: 10.1093/beheco/5.4.362. DOI
Murphey RM, Paranhos da Costa MJR, Gomes da Silva R, de Souza R. Allonursing in river buffalo, Bubalis bubalis: Nepotism, incompetence, or thivery? Anim. Behav. 1995;49:1611–1616. doi: 10.1016/0003-3472(95)90083-7. DOI
Olléová M, Pluháček J, King SRB. Effect of social system on allosuckling and adoption in zebras. J. Zool. 2012;288(2):127–134. doi: 10.1111/j.1469-7998.2012.00930.x. DOI
Hamilton WD. The genetical evolution of social behaviour. II. J. Theor. Biol. 1964;7:17–52. doi: 10.1016/0022-5193(64)90039-6. PubMed DOI
Clutton-Brock TH. Reproductive effort and terminal investment in iteroparous animals. Am. Nat. 1984;123:212–229. doi: 10.1086/284198. DOI
Baldovino MC, Di Bitetti MS. Allonursing in tufted capuchin monkeys (Cebus nigritus): Milk or pacifier? Folia Primatol. 2007;79:79–92. doi: 10.1159/000108780. PubMed DOI
Boness DJ, Craig MP, Honigman L, Austin S. Fostering behavior and the effect of female density in Hawaiian monk seals, Monachus schauinslandi. J. Mammal. 1998;79:1060–1069. doi: 10.2307/1383115. DOI
Cassinello J. Allosuckling behaviour in Ammotragus. Z. Saugetierkd. 1999;64(6):363–370.
Nuñez CM, Adelman JS, Rubenstein DI. A free-ranging, feral mare Equus caballus affords similar maternal care to her genetic and adopted offspring. Am. Nat. 2013;182:674–681. doi: 10.1086/673214. PubMed DOI
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(1):e53052. doi: 10.1371/journal.pone.0053052. PubMed DOI PMC
Zapata B, Gaete G, Correa L, González B, Ebensperger L. A case of allosuckling in wild guanacos (Lama guanicoe) J. Ethol. 2009;27:295–297. doi: 10.1007/s10164-008-0127-7. DOI
Bond ML, Lee DE. Simultaneous multiple-calf allonursing by a wild Masai giraffe. Afr. J. Ecol. 2020;58(1):126–128. doi: 10.1111/aje.12673. DOI
Pratt DM, Anderson VH. Giraffe cowecalf relationships and social development of the calf in the Serengeti. Z. Tierpsychol. 1979;51(3):233–251. doi: 10.1111/j.1439-0310.1979.tb00686.x. DOI
Saito M, Idani G. Suckling and allosuckling behavior in wild giraffe (Giraffa camelopardalis tippelskirchi) Mammal. Biol. 2018;93:1–4. doi: 10.1016/j.mambio.2018.07.005. DOI
Zoelzer F, Engel C, Paul WD, Anna Lena B. A comparative study of nightly allonursing behaviour in four zoo-housed groups of giraffes (Giraffa camelopardalis) J. Zoo Aquar. Res. 2020;8(3):175–180.
Schino G, Aureli F. The relative roles of kinship and reciprocity in explaining primate altruism. Ecol. Lett. 2010;13:45–50. doi: 10.1111/j.1461-0248.2009.01396.x. PubMed DOI
Bercovitch FB, Bashaw MJ, del Castillo SM. Sociosexual behavior, male mating tactics, and the reproductive cycle of giraffe Giraffa camelopardalis. Horm. Behav. 2006;50(2):314–321. doi: 10.1016/j.yhbeh.2006.04.004. PubMed DOI
Bercovitch FB, Berry PSM. Herd composition, kinship and fission—fusion social dynamics among wild giraffe. Afr. J. Ecol. 2013;51(2):206–216. doi: 10.1111/aje.12024. DOI
Carter KD, Seddon JM, Frere CH, Carter JK, Goldizen AW. Fission-fusion dynamics in wild giraffes may be driven by kinship, spatial overlap and individual social preferences. Anim. Behav. 2013;85:385–394. doi: 10.1016/j.anbehav.2012.11.011. DOI
D’haen M, Fennessy J, Stabach J, Brandlová K. Population structure and spatial ecology of Kordofan giraffe in Garamba National Park, Democratic Republic of Congo. Ecol. Evol. 2019;9(19):11395–11405. doi: 10.1002/ece3.5640. PubMed DOI PMC
Horová E, Brandlová K, Gloneková M. The first description of dominance hierarchy in captive giraffe: Not loose and egalitarian, but clear and linear. PLoS ONE. 2015;10(5):e0124570. doi: 10.1371/journal.pone.0124570. PubMed DOI PMC
Jůnková Vymyslická P, Brandlová K, Hozdecká K, Žáčková M, Hejcmanová P. Feeding rank in the Derby eland: Lessons for management. Afr. Zool. 2015;50(4):313–320. doi: 10.1080/15627020.2015.1111167. DOI
Broussard DR, Risch TS, Dobson FS, Murie JO. Senescence and age-related reproduction of female Columbian ground squirrels. J. Anim. Ecol. 2003;72:212–219. doi: 10.1046/j.1365-2656.2003.00691.x. DOI
Cameron EZ, Linklater WL, Stafford KJ, Minot EO. Aging and improving reproductive success in horses: declining residual reproductive value or just older and wiser? Behav. Ecol. Sociobiol. 2000;47(4):243–249. doi: 10.1007/s002650050661. DOI
Cameron EZ, Linklater WL, Stafford KJ, Minot EO. A case of cooperative nursing and offspring care by mother and daughter feral horses. J. Zool. 1999;249:486–489. doi: 10.1111/j.1469-7998.1999.tb01221.x. 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
Birgersson B, Ekvall K. Suckling time and fawn growth in fallow deer (Dama dama) Zoology. 1994;232:641–650.
Fennessy J, Bidon T, Reuss F, Kumar V, Elkan P, Nilsson MA, Vamberger M, Fritz U, Janke A. Multi-locus analyses reveal four giraffe species instead of one. Curr. Biol. 2016;26(18):2543–2549. doi: 10.1016/j.cub.2016.07.036. PubMed DOI
Estes R. The Behavior Guide to African Mammals. University of California Press; 1991.
Altmann J. Observational study of behaviour: Sampling methods. Behaviour. 1974;49:227–267. doi: 10.1163/156853974X00534. PubMed DOI
Špinka M, Illmann G. Suckling behaviour of young dairy calves with their own and alien mothers. Appl. Anim. Behav. Sci. 1992;33(2):165–173. doi: 10.1016/S0168-1591(05)80005-X. DOI
Wright S. Coefficients of inbreeding and relationship. Am. Nat. 1922;56:330–338. doi: 10.1086/279872. DOI