SciELO - Scientific Electronic Library Online

vol.30 issue1Comparison of laboratory methods to assess fiber contents in feedstuffsPre-emptive methadone or tramadol analgesia for mastectomy and ovariohysterectomy in bitches author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand



Related links

  • On index processCited by Google
  • Have no similar articlesSimilars in SciELO
  • On index processSimilars in Google


Revista Colombiana de Ciencias Pecuarias

Print version ISSN 0120-0690

Rev Colom Cienc Pecua vol.30 no.1 Medellín Jan./Mar. 2017 

Original Article

Effect of nursing behavior, sex of the calf, and parity order on milk production of buffaloes1

Efecto del comportamiento de amamantamiento, sexo del becerro y orden del parto sobre la producción de leche en búfalos

Efeito do comportamento de amamentação, sexo do bezerro e ordem de parto sobre a produção de leite em bubalinos

Aparecida de FM Oliveira1  , Celia R Quirino 2   , Rosemary Bastos 2   *  

1Instituto Federal de Educação, Ciência e Tecnologia do Espírito Santo, Alegre, Espírito Santo, Brazil.

2Universidade Estadual do Norte Fluminense “Darcy Ribeiro”, Centro de Ciências e Tecnologias Agropecuárias, Laboratório de Reprodução e Melhoramento Genético Animal, Campos dos Goytacazes, Rio de janeiro, Brazil.



the allonursing effect on daily milk production (DMP) and total milk production (TMP) has been little explored.


to evaluate the effect of nursing behavior, sex of the calf and parity order (PO) on DMP and TMP of buffalo cows.


35 buffalo cows and their calves were evaluated. Observations were performed monthly (three consecutive days) from May to November. The nursing behavior was characterized as: 1) Isolated filial nursing (IFN); 2) Collective filial nursing (CFN), and 3) Non-filial nursing (NFN). Cows were grouped into four categories to study the effects of nursing behavior on DMP and TMP: 1) Non-permissive (NP); 2) Filial permissive (FP); 3) Filial and collective filial permissive (FCFP); and 4) Filial, collective filial and non-filial permissive (FCFNFP). DMP was recorded three days per month and TMP was calculated as DMP*270 days of lactation.


sex of the calf and second and third PO had an effect on nursing behavior (p<0.05). DMP and TMP were significantly affected by calf sex and nursing behavior (p<0.05). PO had no effect on DMP and TMP.


our results suggest that nursing behavior is associated with milk production in buffalo cows. Buffalo cows that accept all types of nursing behavior were had the highest DMP and TMP. Sex of the calf influenced nursing behavior, DMP, and TMP, so that buffalo cows with male calves displayed more frequent allonursing behavior and yielded more milk.

Key words: allonursing; alloparental care; bubalus bubalis; suckling



el comportamiento del alo-amamantamiento sobre la producción diaria de leche (DMP) y producción total de leche (TMP) ha sido poco explorado.


evaluar el efecto del comportamiento de amamantamiento, el sexo del becerro y el orden de parto (PO) en la DMP y TMP de bufalas.


se evaluaron 35 hembras bufalinas y sus crías. Las observaciones se realizaron mensualmente (durante tres días consecutivos) entre mayo y noviembre. El comportamiento de amamantamiento se caracterizó como: 1) Amamantamiento filial aislado (IFN); 2) Amamantamiento filial colectivo (CFN) y 3) Amamantamiento no filial (NFN). Para evaluar los efectos del comportamiento de amamantamiento en la DMP y TMP, las vacas fueron agrupadas en 4 categorías: 1) No permisivas (NP); 2) Permisiva filial (FP); 3) Permisiva filial y colectiva filial (FCFP) y 4) Permisiva filial, colectiva filial y no colectiva (FCFNFP). La DMP se registró tres días por mes, y la TMP fue calculada como DMP*270 días de lactancia.


el sexo del becerro, el segundo y tercer PO tuvieron efecto sobre el comportamiento de amamantamiento (p<0.05). La DMP y la TMP se afectaron significativamente por el sexo del becerro y el comportamiento de amamantamiento (p<0.05). El PO no tuvo efecto sobre la DMP y la TMP.


nuestros resultados sugieren que el comportamiento de amamantamiento está asociado a la producción de leche en vacas bubalinas. Las bufalas permisivas a todo tipo de amamantamiento presentaron mayor DMP y TMP. El sexo del becerro influyó en el comportamiento de amamantamiento, en la DMP y en la TMP. Las bufalas con becerro macho presentaron comportamiento de alo-amamantamiento más frecuente y produjeron mayor cantidad de leche.

Palabras-clave: alo-amamantación; bubalus bubalis; cuidado aloparental; lactación



o comportamento de alo-amamentação sobre a produção de leite diária (DMP) e produção de leite total (TMP) tem sido pouco explorado.


avaliar o efeito do comportamento de amamentação, sexo dos bezerros e ordem de parto (PO) na DMP e TMP em vacas bubalinas.


trinta e cinco fêmeas e suas crias foram avaliadas no estudo. As observações foram realizadas mensalmente (três dias consecutivos) de maio a novembro. O comportamento de amamentação foi caracterizado como 1) amamentação filial isolada (IFN); 2) amamentação coletiva filial (CFN) e 3) amamentação não filial (NFN). Para avaliar os efeitos do comportamento da amamentação na DMP e TMP, as vacas bubalinas foram agrupadas em 4 categorias: 1) não permissiva (NP); 2) permissiva filial (FP); 3) permissiva filial e coletiva filial (FCFP) e 4) permissiva filial, coletiva filial e não filial (FCFNFP). A DMP foi registrada três dias para cada mês e a TMP foi calculada como DMP*270 dias de lactação.


o sexo dos bezerros, a segunda e terceira PO tiveram efeitos no comportamento de amamentação (p<0.05). A DMP e TMP foram significativamente afetadas pelo sexo dos bezerros e comportamento de amamentação (p<0.05). A PO não teve efeito na DMP e TMP.


nossos resultados sugerem que o comportamento de amamentação estão associados a produção de leite em vacas bubalinas. As vacas bubalinas que são permissíveis a todos os tipos de amamentações foram aquelas com maior DMP e TMP. O sexo dos bezerros influenciou o comportamento de amamentação, DMP e TMP, sendo que as vacas bubalinas que possuem bezerros machos apresentaram frequente comportamento de alo-amamentação e produziram maiores quantidades de leite.

Palavras-Chave: alo-amamentação; bubalus bubalis; cuidado aloparental; mamada


In some species, during the nursing period lactating females occasionally nurse offspring that are not their own, a behavior referred to as allonursing (Riedman, 1982; Hoogland et al., 1989). Allonursing can contribute to maternal welfare, udder health and milk quality by reducing painful milk pressure and udder infections, which maximizes milk production (Roulin, 2002).

One of the great benefits for allosucklers is the compensation of some important deficiencies at birth, such as low birth weight or maternal milk insufficiency (Víchová and Bartos, 2005). Allosucklers may also gain immunological benefits by suckling from more than one nursing mother thus obtaining various specific immunological compounds, which improve resistance against pathogens (Roulin and Heeb, 1999). Besides this, allosucklers can also ingurgitate extra milk and thereby obtain additional energy (Packer et al., 1992). However, allonursing may imply costs, because lactation is the most energetically expensive stage in mammals (Clutton-Brock et al., 1989). In addition, milk transfer could reduce the amount of nutrients available to the current calf (Mendl, 1988) and allonursing can spread pathogens to a number of calves simultaneously (Roulin and Heeb, 1999).

Some non-mutually exclusive hypotheses have been proposed to explain why lactating females nurse alien offspring: misdirected parental care (Packer et al., 1992); reciprocity (Ekvall, 1998; Engelhardt et al 2015; Glonekov et al., 2016); kin selection (Pusey and Packer, 1994; Ekvall, 1998; Eberle and Kappeler, 2006; Engelhardt et al., 2016); evacuation of leftover milk (Riedman and Le Boeuf, 1982; Wilkinson, 1992); inexperience of females (Murphey et al., 1991, 1995), and milk theft (Murphey et al., 1995; Maniscalco et al., 2007; Zapata et al.,2009; Engelhardt et al., 2014; Glonekov et al., 2016).

In buffaloes, the allonursing behavior was first observed in a feral herd of Carabao buffalos (Tulloch, 1979) and was also subsequently reported by Murphey et al. (1991; 1995), Paranhos da Costa et al. (2000), Andriolo et al. (2001) and Madella-Oliveira et al. (2010). The effects of calf sex and birth order in buffaloes can decisively influence social interactions during sucking, promoting differential development among calves (Paranhos da Costa et al., 2000). In the Iberian red deer (Cervus elaphus hispanicus), the comparison between hind milk production (MP) and allosucking frequency shows that the percentage of allosucking bouts increases as the MP of the nursing mothers decreases (Landete-Castillejos et al., 2000).

The objective of this study was to evaluate the potential effects of the calf sex and parity order (PO) on nursing behavior, DMP, and TMP of buffalo cows.

Materials and methods

Ethical considerations

The experimental protocol was reviewed and approved by the Ethics Committee on Animal Use of Universidade Estadual do Norte Fluminense Darcy Ribeiro, Brazil (approval number: 262/2014)

Location and animals

The study was conducted at Cataia farm in São Francisco do Itabapoana, Rio de Janeiro, Brazil (21º18’07” S and 40º57’41” W, at an altitude of 8 meters above sea level). In this study, outbred Murrah, Jaffarabadi and Mediterranean females (n= 35; aged 3 to 12 years old) and their calves were investigated. The group included primiparous (n= 2) and multiparous females (n= 33). Calves (15 males and 20 females) included in the study were all born in March (n= 14), April (n= 9) and May (n= 12).

Dams and calves were individually identified with yellow oil paint, with ordinary numbers painted on the hindquarters. Matching numbers were assigned to the cow and calf; so they could be identified from a distance. Plastic earrings were put on the animals, so that they were permanently identified. The animals were habituated to the horseback observer inside pasture for at least 15 days before beginning data collection. During this period, the observer conducted the training using a protocol. Following the farm routine, each cow and her calf were allocated for 15 days in a maternity pasture system (separated from other females). Milking began at 4:00 h, when females were manually milked in the presence of their calves. After milking, around 6:00 h, the herd was conducted to the pasture (measuring 60 hectares), where all females remained with their calves until 12:00 h. The stocking rate used was 0.73AU/ha. The herd was removed at 12:00 h and the mothers were then placed in a pasture away from their calves.

Data were collected during three days at the beginning of each month (May to November). Observations were direct and continuous between 6:00 and 12:00 h (Martin and Bateson, 1986). The observer was in a distance of around 10 m from the animals. A binocular was used for identification of numbers at a distance, to avoid interference with the behavior of the animals. All animals were in sight at all times. A timer was used to register nursing time, followed by identification of the cow and calf. The timing of the start and end of nursing was registered in an audio recorder. Nursing was considered to begin from the moment the calf attached to the teat with a suckling movement.

Nursing behavior was characterized into three types: 1) Isolated filial nursing (IFN): when the female was nursing its own calf; 2) Collective filial nursing (CFN): when a female began nursing its own calf as well as one or more alien calves; and 3) Non-filial nursing (NFN), when a female was nursing one or more calves that were not hers.

To study the effect of nursing behavior on daily milk production (DMP) and total milk production (TMP), females were grouped into four categories: 1) Non-permissive (NP): females that did not allow any kind of nursing; 2) Filial permissive (FP): females that allowed IFN; 3) Filial and collective filial permissive (FCFP): females that allowed two types of nursing behavior: IFN and CFN; and 4) Filial, collective filial and non-filial permissive (FCFNFP): females that allowed three types of nursing behavior: IFN, CFN and NFN.

Milk was collected from each cow and quantified during the same three days per month when nursing behavior was observed. DMP was registered in kilograms. TMP was defined as the amount of milk (kg) produced throughout the lactation period (270 days).

Statistical analysis

The data were analyzed using SAS (SAS Institute Inc, Cary, NC, USA). Frequency of behavior was analyzed with the chi-square test (PROC FREQ). For other data, we used PROC MIXED to fit a linear model for repeated measures. Animal was used as the random effect, while nursing behavior, sex of calf, month of observation and parity order were fixed effects. Results are reported as least square means (LSMEANS) with standard error (SE) given by the PROC MIXED. We used p≤0.05 as the level of statistical significance for all tests.

The analysis model was as follows:


Yijklm = daily milk production and total milk production.

( = general average.

TMi = effect of i th nursing behavior.

Sj = effect of sex of the j th calf.

MOk = effect of kth month of observation.

POl = effect of lth parity order.

an = random effect of animal.

eijklm = random error associated with each observation (N ~ 0.1).


Nursing behavior

Results in Table 1 show no difference in duration of nursing between buffalo cows with male or female calves. Frequency and duration of nursing behavior for the IFN were significantly greater in relation to CFN and NFN (p<0.05). There was also significant difference in relation to frequency and duration for CFN and NFN (p<0.05). Frequency of nursing was greater in buffalo cows with male calves (p<0.05) than cows with female calves (Table 1).

Differences in frequency and duration of nursing behavior were observed (p<0.05). In May, frequency of nursing behavior was significantly greater compared with June, September and November, and duration of nursing behavior was higher compared with June, September, October and November (p<0.05). A significant difference for frequency of nursing behavior was observed between November and July, August, October (p<0.05). Regarding duration of nursing behavior, a difference was observed between November and the other months (p<0.05).

For the PO among buffalo cows there were statistically significant differences in frequency and duration of nursing behavior (p<0.05). Buffalo cows in 2nd and 3rd PO had greater frequency values of nursing behavior compared with cows in 1st and 4th PO. Regarding duration of nursing behavior, cows in 2nd and 3rd PO had greater values compared with the other POs (p<0.05).

Table 1 Least square means and standard errors (SE) for frequency (episode/day) and duration (seconds/day) of nursing type allowed by buffalo cows, calf sex , month, and parity order (PO).  

IFN: isolated filial nursing; CFN: collective filial nursing and NFN: non-filial nursing. N: number of observations. Means followed by different superscript letters (a, b, c) within the same column are significantly different (p<0.05)

Nursing behavior in relation to calf sex and PO

Figure 1 shows that frequency (A) and duration (B) of IFN were significantly greater in

relation to CFN and NFN for both cows with male or female calves (p<0.05). A significant difference was found in relation to duration (B) for CFN and NFN for both cows with male and female calves (p<0.05), but not for frequency.

Results show that frequency (A) of IFN was higher for b cows with male than those with female calves (p<0.05) for each nursing type,. Cows with female calves showed higher values for duration (B) of IFN than those with male calves (p<0.05). Besides, frequency (A) and duration (B) of nursing behavior for CFN were significantly greater in relation to NFN when comparing cows with male versus female calves (p<0.05).

Figure 1 Least square means and standard errors (SE) of the (A) frequency (episode/day) and (B) duration (seconds/day) of each nursing type in relation to sex of the calf. IFN: isolated filial nursing; CFN: collective filial nursing and NFN: non filial nursing. Means with different superscript lowercase letters (a, b, c) show significant difference between nursing types (p<0.05) and means with different superscript uppercase letters (A, B) show significant difference between calf sex with regards to nursing type (p<0.05). 

Figure 2 shows the frequency (A) and duration (B) of types of nursing behavior in relation to PO. Except for the second PO, which showed no difference in frequency between IFN and CFN, the frequency and duration of IFN were statistically significant when compared with CFN and NFN for all POs (p<0.05).

Figure 2 Least square means and standard errors (SE) of (A) frequency (episode/day) and (B) duration (seconds/day) of each nursing type in relation to PO. IFN: isolated filial nursing; CFN: collective filial nursing and NFN: non filial nursing. PO: parity order. Means followed by different superscript letters (a, b) are significantly different within each PO (p<0.05).  

Factors affecting DMP and TMP: nursing behavior, calf sex, month of observation, and PO.

Table2 Least square means and standard errors (SE) of daily milk production (DMP) and total milk production (TMP) in relation to nursing behavior, sex of calves, month of observation and parity order (PO) in buffalo cows. 

Nursing behavior: NP: non-permissive; FP: filial permissive; FCFP: filial and collective filial permissive and FCFNFP: filial, collective filial and non-filial permissive. N: number of observations. Means followed by the different superscript letters (a, b, c, d, e) within the same column are significantly different (p<0.05).

The average lactation length for these animals was 213.42 days, with a standard deviation of 66.11 days. The DMP and TMP in relation to nursing behavior, calf sex, month, and PO in cows are shown in Table 2.

The nursing behavior among the 35 buffalo cows was distributed as follows: 3 were NP, 18 FP, 7 FCFP and 7 FCFNFP. As shown, DMP and TMP for cows with FCFNFP were significantly higher compared to those with NP, FP and FCFP (p<0.05).

The DMP and TMP in cows with male calf were significantly greater than that of cows with female calf (P<0.05). During the observed months, the peak of DMP and TMP occurred in May. A decrease in DMP and TMP was observed from June to November (Table 2). The PO among cows did not have an effect on DMP nor on TMP (Table 2).


Our results show that collective nursing occurr in buffalo cows, in agreement with other studies (Murphey et al., 1991; 1995; Paranhos da Costa et al., 2000; Andriolo et al., 2001). The IFN values for frequency and duration were higher than CFN and NFN, different than reported by Andriolo et al. (2001), who observed lower values for occurrence and duration of IFN compared to CFN. The low values for collective nursing suggest that farm management interferes with this behavior.

The sex of the calf had an effect on nursing behavior; cows with male calves displayed greater nursing frequency than the ones with female calves, and the frequency and duration of IFN for both were more evident compared with other nursing types (CFN and NFN). Paranhos da Costa et al. (2000) demonstrated that male calves spend greater time in individual filial and in communal non-filial suckling than female calves, which shows greater communal filial suckling, suggesting that the sex of the offspring determines differences in allonursing strategies. In bovine cattle, calf sex had no effect on allosucking frequency and growth gain of the calves (Víchová and Bartŏs, 2005). Zapata et al. (2010) demonstrated that the relationship between allosuckling and the offspring sex was not evident in guanacos ( Lama guanicoe) .

Nursing behavior was more prevalent in May, July and August. Andriolo et al. (2001) showed that suckling behavior varied according to the period of observation. There were increased suckling and decreased filial suckling during the first four months, while a decrease following the gradual process of weaning was observed after the fourth month of nursing. .

Our results showed differences in duration of nursing behavior for cows in 2nd and 3rd PO. The frequency and the duration of IFN were higher when compared with CFN and NFN in all POs, except for the second PO. This indicates the importance of filial nursing to ensure calf nutrition. According to Gloneková et al. (2016), not only female parity affects the probability of successful suckling involving non-filial calves, but also the order of calf suckling (which calf came to suckle first, second, etc.). Thus, other variables should be evaluated, such as age of the calf, age of the nursing female, and hierarchy rank differences between the nursing female and the own mother of the calf.

Our results show that cows that were permissible to all types of nursing behavior (filial, collective filial and non-filial) presented higher DMP and TMP. We thus infer that cows permitting more than one nursing behavior are more stimulated to produce more milk. The cow-calf interaction is important to release oxytocin, a hormone that stimulates milk ejection (Pollack and Hurnik, 1978). In bovine cows, Silveira et al. (1993) demonstrated that the frequency of oxytocin release following suckling was greater in the own group when compared to the alien group, thus the release of oxytocin was affected by mother-young bonds.

In the Iberian red deer, the percentage of allonursing bouts increased with increasing milk production by the nursing hind, but the percentage of allosuckling bouts increased as milk production of the mother decreased (Landete-Castillejos et al., 2000), which shows a difference between nursing behavior of the female and suckling behavior of the calf in relation to milk production.

Furthermore, cows with male compared with female calves showed higher DMP and TMP. This is in agreement with Landete-Castillejos et al. (2005), who showed that for Iberian red deer calves milk yield was greater in dams with males than in dams with females. However, different results were described by Paranhos da Costa et al. (2000) who did not observe a significant relationship between milk production and sex of the calf.

The peak of DMP and TMP occurred in May. From June to November, DMP and TMP decreased. DMP was 6.9 ± 0.3 kg/day in May, but at the beginning of June, production began to decline until November, reaching 2.7 ± 0.3 kg/day. Cerón-Muñoz et al. (2002) showed that production in the first month of lactation was 6.87 kg, declining until the ninth month of lactation, with 3.83 kg. Hurtado-Lugo et al. (2005) obtained high values at the beginning of lactation (4.64 kg to 3.04 ± 1.17 kg). We observed that TMP ranged from 1853.0 ± 76.2 (May) to 739.9 ± 80.8 (November) kg. Sampaio Neto et al. (2001) reported total milk production of 2130.80 ± 535.60 kg, and Junior et al. (2014) found a value of 2218.03 kg.

Our results did not show a definite propensity for a change in the pattern of DMP and TMP related to PO. These results are not in agreement with Sampaio Neto et al. (2001), Afzal et al. (2007) and Pawar et al. (2012), because these studies showed DMP was affected by female parity. The fact that we did not find a difference between PO and DMP and TMP may be related to the quality of the pasture, since pastures are native, with low nutritional quality, and no other supplementary feed was provided to the animals.

In addition, genetic and non-genetic traits should be taken into consideration for milk production parameters. Genetic improvement is related to selection, while non-genetic factors involve management, quantity and quality of feed, and season (Afzal et al., 2007).

In conclusion, our results suggest that nursing behavior is associated with milk production in buffalo cows. Females that are permissible to all types of nursing behavior had the highest DMP and TMP. The sex of calves influenced nursing behavior, DMP and TMP, so cows with male calves displayed more frequent allonursing behavior and produced higher amounts of milk. Females can present different types of nursing behavior, independent from PO, but IFN was more evident in all POs. The DMP and TMP were not affected by PO.


To Mr Aloísio Siqueira de Almeida, farm owner, and his assistants, for allowing us to conduct the experiment, and FAPERJ for financial support (grant No. E-26/170.645).

Conflicts of interest

The authors declare they have no conflicts of interest with regard to the work presented in this report


Afzal M, Anwar M, Mirza MA. Some factors affecting milk yield and lactation length in Nili Ravi buffaloes. Pakistan Vet J 2007; 27(3):113-117. [ Links ]

Andriolo A, Paranhos da Costa MJR, Schmidek WR. Suckling behaviour in water buffalo (Bubalus bubalis): developement and individual differences. Revist Etol 2001; 3(2):129-136. [ Links ]

Cerón-Muñoz M, Tonhati H, Duarte J, Munõz-Berrocal M, Jurado-Gámez H. Factors affecting somatic cell counts and their relations with milk and milk constituent yield in buffaloes. J Dairy Sci 2002; 85:2885-2889. [ Links ]

Clutton-Brock TH, Albon, SD, Guinness FE. Fitness cost of gestation and lactation in wild mammals. Nature 1989; 337:260-262. [ Links ]

Eberle, M, Kappeler, PM. Family insurance: kin selection and cooperative breeding in a solitary primate (Microcebus murinus). Behav Ecol Sociobiol 2006; 60:582-588. [ Links ]

Ekvall K. Effects of social organization, age and aggressive behavior on allosuckling in wild fallow deer. Anim Behav 1998; 56:695-703. [ Links ]

Engelhardt SC, Weladji RB, Holand O, Rioja CM, Ehmann RK, Nieminen M. Allosuckling in reindeer (Rangifer tarandus): milk-theft, mismothering or kin selection? Behav Processes 2014; 107:133-141. [ Links ]

Engelhardt SC, Weladji RB, Holand O, Roed KH, Nieminen M. Evidence of reciprocal allonursing in reindeer, Rangifer tarandus. Ethology 2015; 121:245-259. [ Links ]

Engelhardt SC, Weladji RB, Holand O, Nieminen M. Allosuckling in reindeer (Rangifer tarandus): a test of the improved nutrition and compensation hypotheses. Mamm Biol 2016; 81:146-152. [ Links ]

Gloneková M, Brandlová K, Pluhácek J. Stealing milk by young and reciprocal mothers: high incidence of allonursing in giraffes. Giraffa cameloparalis. Anim Behav 2016; 113: 113 -123. [ Links ]

Hoogland JL, Tamarim RH, Levy CK. Communal nursing in prairie dogs. Behav Ecol Sociobiol 1989; 24(2):91-95. [ Links ]

Hurtado-Lugo N, Cerón-Muñoz M, Tonhati H Gutierrez-Valencia A, Henao A. Producción de leche em búfalas de la Costa Atlántica Colombiana. Livest Res Rural Develop 2005; 17:12. [ Links ]

Junior JSB, Fraga AB, Couto AG, Barros CC, Silva RMO. Produção de leite, duração da lactação e intervalo de partos em búfalas mestiças Murrah. Rev Caatinga 2014; 27(2):184-191. [ Links ]

Landete-Castillejos T, Garcia A, Garde J, Gallego L. Milk intake and production curves and allosuckling in captive Iberian red deer, Cervus elaphus hispanicus. Anim Behav 2000; 60:679-687. [ Links ]

Landete-Castillejos T, Garcia A, López-Serrano FR, Gallego L. Maternal quality and differences in milk production and composition for male and female Iberian red deer calves (Cervus elaphus hispanicus). Behav Ecol Sociobiol 2005; 57:267-274. [ Links ]

Madella-oliveira AF, Bastos R, Quirino CR. Comportamento de amamentação e mamada em bubalinos, suas relações com período de lactação, idade e sexo dos bezerros. Rev Ceres 2010; 57(2):211-217. [ Links ]

Maniscalco JM, Harris KR, Atkinson S, Parker P. Alloparenting in Steller sea lions (Eumetopias jubatus): Correlations with misdirected care and other observations. J Ethol 2007; 25(2):125-131. [ Links ]

Martin P and Bateson P. Measuring Behaviour and introductory guide. Cambridge: Cambridge University Press, 1986. [ Links ]

Mendl M, 1988. The effects of litter size variation on mother-offspring relationships and behavioural and physical development in several mammalian species (principally rodents). J Zool (Lond) 1988; 215:15-34. [ Links ]

Murphey RM, Paranhos da Costa MJR, Lima LOS, Duarte FAM. Communal sucking in water buffalo (Bubalus bubalis). Appl Anim Behav Sci 1991; 28:341-352. [ Links ]

Murphey RM, Paranhos da Costa MJR, Gomes da Silva R, Souza RC. Allonursing in river buffalo, Bubalus bubalis: nepotism, incompetence, or thievery? Anim Behav 1995; 49 (6):1611-1616. [ Links ]

Packer C, Lewis S, Pusey A. A comparative analysis of non-offspring nursing. Anim Behav 1992; 43(2):265-281. [ Links ]

Paranhos da Costa MJR, Andriollo A, Oliveira JFS, Schimidek WR. Suckling and allosuckling in river buffalo calves and its relation with weight gain. Appl Anim Behav Sci 2000; 66(1):1-10. [ Links ]

Pawar HN, Ravi Kumar GVPPS, Narang R. Effect of year, season and parity on milk Production traits in Murrah buffaloes. J Buffalo Sci 2012; 1:122-125. [ Links ]

Pollack WE, Hurnik JF. Effect of calf calls on rate of milk release of dairy cows. J Dairy Sci 1978; 61:1624-1626. [ Links ]

Pusey AE, Packer C. Non-offspring nursing in social carnivores: minimizing the costs. Behav Ecol 1994; 5(4):362-374. [ Links ]

Riedman ML, Le Boeuf BJ. Mother-pup separation and adoption in northern elephant seals. Behav Eco Sociol 1982; 11(3):203-215. [ Links ]

Roulin A, Heeb P. The immunological function of allosuckling. Ecol Lett 1999; 2(5):319-324. [ Links ]

Roulin A. Why do lactating females nurse alien offspring? A review of hypothese and empirical evidence. Anim Behav 2002; 63(2):201-208. [ Links ]

Sampaio Neto, JC, Martins Filho, R, Lôbo, RNB, Tonhati, H. Avaliação dos desempenhos produtivos e reprodutivos de um rebanho bubalino no Estado do Ceará. R Bras Zootec 2001; 30(2):368-373. [ Links ]

SAS - Institute Inc. Statistical Analysis System user’s guide. Version 9.3 ed. SAS Institute Inc. Cary, North Carolina, USA, 2012. [ Links ]

Silveira PA, Spoon RA, Ryan DP, Williams GL. Evidence for maternal behavior as a requisite link in suckling-mediated anovulation in cows.1993; 49(6):1338-1346. [ Links ]

Tulloch DG. The water buffalo, Bubalus bubalis, in Australia: Reproductive and parent-offspring behaviour. Aust Wildlife Res 1979; 6(3):265-287. [ Links ]

Víchová L, Bartoš L. Allossuckling in cattle: Gain or compensation? Appl Anim Behav Sci 2005; 94:223-235. [ Links ]

Wilkinson GS. Communal nursing in the evening bat, Nycticeius humeralis, Behav Ecol Sociobiol 1992; 31:225-235. [ Links ]

Zapata B, Correa L, Soto-Gamboa M, Latorre E, González, BA, Ebensperger LA . Allosuckling allows growing offspring to compensate for insufficient maternal milk in farmed guanacos (Lama guanicoe). Appl Anim Behav Sci 2010; 122:119-126. [ Links ]

Zapata B, González, BA, Ebensperger LA . Allonursing in captive guanacos, Lama guanicoe: Milk theft or misdirected parental care? Ethology 2009; 115:731-737. [ Links ]

1To cite this article: Oliveira AFM, Quirino CR, Bastos R. Effect of nursing behavior, sex of the calf, and parity order on milk production of buffaloes. Rev Colomb Cienc Pecu 2017; 30:30-38

Received: September 18, 2015; Accepted: September 09, 2016

* Corresponding author: Rosemary Bastos. Laboratório de Reprodução e Melhoramento Genético Animal, Centro de Ciências e Tecnologias Agropecuárias, Universidade Estadual do Norte Fluminense “Darcy Ribeiro”, Av. Alberto Lamego, 2000, CCTA - P4 - laboratório 01 térreo - Parque Califórnia, Campos dos Goytacazes, RJ, Brasil, Cep: 28016-812. Tel.: +55-2227397196. E-mail:

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License