Fighting for Colostrum
2006), stimulating intestinal development (see review by Farmer et al. 2006) and providing maternal immunoglobulin [IG] (particularly immunoglobulin G [IgG] in colostrum), which ‘equips’ the young of many mammalian species (especially important in ungulates) with passive immune protection (see reviews by Rooke & Bland 2002; Mellor & Stafford 2004; Baintner 2007; Day 2007). However, colostrum does not have the same importance for passive immunity of all mammals. The importance of colostrum depends on the ‘route’ of maternal antibody transfer to the offspring. This transfer can be prenatal, through the chorioallantoic placenta or yolk sac wall (exclusive prenatal IG transfer can be found in primates and lagomorphs), or post-natal from colostrum via the intestinal wall (exclusive post-natal IG transfer can be found in ungulates and opossums) (review in Baintner 2007). Some mammals (carnivores and rodents) transfer IG both pre- and postnatally (Baintner 2007; Langer 2009). For instance, in cats and dogs, shortness of the gut is compensated by prenatal IG transmission (Baintner 2007). The importance of post-natal IG transfer via colostrum is relatively low in mammals with prenatal passive immunisation. If prenatal IG transfer is inhibited (e.g. ungulates), large quantities of IG must be available post-natally (Langer 2009). The mechanism of IG transfer is reflected in the differences between the composition of colostrum and mature milk. In some mammals (e.g. ungulates), colostrum and mature milk are considerably different in their compositions. In other mammals (e.g. primates, rodents and lagomorphs), the compositions of colostrum and mature milk are similar. In ungulates and dogs, substantially richer protein content is observed in colostrum than in milk, whereas in some other mammals (e.g. rats and cats), mature milk contains more proteins than colostrum (reviewed by Langer 2009). Therefore, competition (fighting) for colostrum could be of vital importance for some mammalian species, especially pigs, which are the only truly multiparous ungulates (Estes 1991). Costly fighting would not confer considerable fitness benefits for other species such as the domestic dog Canis lupus familiaris, the European rabbit Oryctolagus cuniculus and many rodent species, which show little or no agonistic behaviour during suckling (reviewed by Hudson & Distel 2013). However, in ungulates, the quantity and duration over which colostrum is produced by the mother is limited, and there are limitations to the physiological ability of offspring to optimise the passive immunity provided by colostrum.
First, it should be noted that colostrum is only produced for a short time after parturition (up to 48 h); hence, it is limited in terms of quantity. Previous studies have demonstrated that the litter size of domestic pigs does not influence colostrum yield. In other words, there is an upper quantitative limit in colostrum production by the sow; therefore, piglets from large litters have less colostrum available on the individual basis (e.g. Devillers et al. 2007). The second important limitation related to colostrum is the capacity of the neonate small intestine to absorb intact immunoglobulins. Immunoglobulins are normally only available for a short period before gut closure after birth, at which point the capacity to absorb intact antibodies is lost. Gut closure normally coincides with the period of colostrum production, taking place up to 48 h after birth. In piglets, gut closure usually occurs up to 24 h after birth (see reviews by Rooke & Bland 2002; Mellor & Stafford 2004). In addition, there is a major drop in IgG production within 12 h of the onset of farrowing (Klobasa et al. 1987; Devillers et al. 2004). Farrowing lasts for an average of 3 h and, potentially, about 8 h (Van Dijk et al. 2005). Based on these limitations associated with colostrum, it is not surprising that the majority of suckling fights by piglets occur within the first day after farrowing, and by the second day, the number of teat disputes is halved (De Passille et al. 1988a); however, this behaviour does not hold for kittens, which maintain similar levels of contests throughout lactation (Hudson et al. 2009). Colostrum is not of particular importance for passive immunity of kittens because of prenatal IG transfer. In addition, mature milk in cats has relatively more proteins, fats and carbohydrate (lactose) than that in colostrum (reviewed by Langer 2009). The composition (richness) of mature milk may contribute to sustained levels of fighting among kittens throughout lactation. Although the frequency of teat disputes tends to be negatively correlated with weight gain, De Passill e et al. (1988a) found that the greatest number of teat disputes that a piglet won on the first day of lactation significantly increased their weight gain in the first 3 d of lactation. Moreover, colostrum ejection occurs as each individual piglet is born (Broom 1983). Thus, as each additional piglet is born, the struggle (fights) for teats/colostrum (which is permanently available throughout farrowing) is probably amplified. The ability of piglets to compete (fight) for teats is of great importance, especially for late-born piglets. Although these piglets tend to weigh slightly more at birth than piglets born earlier, they also tend consume slightly
Ethology 120 (2014) 1–6 © 2014 Blackwell Verlag GmbH2
Fighting During Suckling: Is it Really an Epiphenomenon? J. Skok & D. Skorjanc
less colostrum (Fraser & Rushen 1992) and have relatively low serum IgG concentrations (De Passille et al. 1988b). In addition, De Passille et al. (1988b) reported that piglets that engage in a very low frequency of suckling bouts have low serum IgG levels. Therefore, a stronger (and more aggressive) neonatal competitor may acquire more early colostrum that is rich in immunoglobulins because it is able to successfully occupy and exploit more than one teat. Consequently, these individuals have a greater chance of survival, in addition to their fitness being enhanced; this benefits their later reproductively active life stage. Therefore, natural selection should favour the neonatal tendency to fight for teats to allocate resources, thus ensuring that the largest and most healthy offspring survive (Andersen et al. 2011). Indeed, colostrum intake represents the main factor for piglet survival, through the provision of energy and immune protection (e.g. Herpin et al. 2002; Farmer et al. 2006; Devillers et al. 2011). Thus, piglets should strive to ingest sufficient amounts of colostrum as soon as possible after birth, as it literally translates into a life-and-death struggle. Therefore, costly fighting represents a trait with momentary functional value in the competition for colostrum. However, unrestricted fighting over teats does not confer a fitness benefit. Therefore, a certain level of suckling orderliness is essential because it reduces exaggerated teat disputes and the risk of missed suckling opportunities (De Passille et al. 1988a,b). Skok and Skorjanc (2014) reported that the process of teat-order formation in piglets, which is generally completed in the second week of lactation, normally starts as group suckling cohesion immediately after farrowing. The authors further reported that mortality was higher in litters in which teat-order formation was somehow disturbed and delayed than in litters in which teatorder formation was initiated early.