Introduction

Among mammals, lactation is the most energy demanding part of parental care [1], so parent-offspring conflict [2] is expected over milk provided by the mother. In particular, parent and offspring should disagree over how long the period of the parental investment should last and over the amount of parental investment that should be provided [2].

In some species, females commonly become pregnant shortly after parturition of previous young, which further intensifies mother-offspring conflict due to concurrent pregnancy and intensive lactation, e.g., in many small rodents and lagomorphs [3]–[5] or some ungulate species, including equids [6]–[8]. In horses, lactating mares under natural conditions usually get pregnant again during the first or second oestrus after giving birth (e.g., [6], [7], [9] post-partum mares experience oestrus, commonly called “foal heat”, during the first week after birth [9].

The mares of free living horses [6], [10], [11] follow the general assumption that the optimum weaning time for pregnant mothers conceiving shortly after giving birth should be earlier than for non-pregnant ones [12]. Earlier weaning in pregnant mares was apparent even in plains zebra mares kept in captivity under optimal nutritional conditions [13]. Females of equid species time weaning according to the expected date of next delivery [7], [11], [13], [14].

While these studies demonstrate well the crucial impact of pregnancy in lactating equid female on mother-offspring conflict over the period of the parental investment (i.e., weaning conflict), little is known about how mother's pregnancy influences conflict between the mother and her offspring over the amount of parental investment she provides during lactation. It was found only recently that in captive plains zebra there are shorter suckling bouts in pregnant mares than non-pregnant ones, suggesting higher mother-offspring conflict when the mother was pregnant [15].

Although suckling behaviour was not found a reliable indicator of milk or energy intake [16], even in foals [17], it can be considered as the behavioural measure associated with parent-offspring conflict over maternal resources [16], [17] and as the measure of the level of maternal care provided by the mother in contrast with foal's needs [10], [18], [19]. Termination of suckling seems to be of great importance. Suckling bouts terminated by the mother are usually shorter compared to those terminated by the foal [15], [20]. As such, it probably indicates that the foal was not satiated [17].

In the present study, we tested effect of pregnancy on suckling behaviour variables as indicators of mother-offspring conflict in domestic horses. We hypothesised shorter suckling bouts and higher rates of rejected and/or terminated suckling in pregnant mares compared to non-pregnant ones caused by increased conflict over amount of maternal investment between mother and her nursed young are to be expected because of her parallel investment into two offspring, a nursed foal and a foetus.

Methods

Results

Within 516 hours of observation of 79 mare-foal pairs we recorded 10 848 suckling solicitations, from which 10 607 resulted in a suckling bout. The mothers terminated 14.96% of suckling bouts. Suckling bout duration ranged between 5 and 198 s (mean ± SE: 73.8±28.9 s). Suckling bouts terminated by the mother were considerably shorter than those the foal terminated itself (62.96±0.89 s vs. 76.93±0.61 s, F_{(1, 9776)} = 319.6, P<0.0001, GLMM, PROC MIXED, SAS).

We found no significant effect of pregnancy on probability of the mother rejecting suckling solicitation of her foal (n. s., GzLM, PROC GENMOD, SAS). Nevertheless, sucking attempts rejected by the mother accounted just for 1.0% of observed suckling solicitations and the predicted probability did not exceed 0.028 so they did not seem to be generally of great importance in our case. There was also no significant effect of pregnancy of the mother on the probability of her terminating a suckling bout (n. s., GzLM, PROC GENMOD, SAS).

Neither frequency of suckling solicitations (13.2±5.11, mean ± SD, ranging from 1 to 40 suckling solicitations per observation day) nor suckling bouts (13.0±5.01, ranging from 1 to 38 suckling bouts per observation day) were influenced by reproductive status of the mother (n.s., GLMM, PROC MIXED, SAS).

However the overall effect of mother's pregnancy on suckling bout duration was not significant (70.99 s in pregnant vs. 68.90 s in non-pregnant mares, n. s., GLMM, PROC MIXED, SAS), there were considerable differences in pregnant and non-pregnant mares when taking into account who terminated a suckling bout, whether the mother or the foal (interaction pregnancy*terminator: F_{(1, 9776)} = 12.1, P<0.001). In case of the mother terminated a suckling bout the suckling bouts were longer in pregnant (65.36±1.25 s) than in non-pregnant mares (60.55±1.36 s) while there was no impact detected of pregnancy on duration of suckling bouts terminated by the foal (76.62±0.90 s vs. 77.24±0.94 s, n. s.; see Fig. 1). We found no general correlation between suckling bout duration and frequency (partial r_s = −0.03, n.s., with age of the foal eliminated).

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Figure 1. Suckling bout duration [s] according to the reproductive status of the mother when suckling bouts terminated the mother (left) or the foal (right).

(Differences between categories including different terminator of a suckling bout were all P<0.0001.)

https://doi.org/10.1371/journal.pone.0022068.g001

Birth weight of the foals born within the season following observations of suckling behaviour did not differ in foals of lactating (66.2±1.01 kg) and non-lactating mares (64.4±1.04 kg, F_{(1, 72)} = 1.55, P = 0.22).

Discussion

We found that domestic horse mares in some aspects altered their nursing behaviour during period of intensive lactation according to whether they were pregnant or not. Contrary to our predictions, however, we haven't found any signs of maternal care shortening towards nursed foals in pregnant mares which would be expected considering concurrent investment of a female into two offspring, a nursed offspring and a foetus; we found quite the opposite.

Pregnant mares did not either reject the foals' attempts to suck nor have they terminated suckling bout more often than non-pregnant nursing females, indicating no conflict between mother and offspring over suckling controlled by pregnancy. Considering negligible amount of suckling solicitation the mothers rejected (1% from suckling solicitations of the foals) it was predominantly through termination of suckling bouts (15% from successful suckling bouts) how the mares controlled the amount of maternal resources they provided to their nursed young. As expected, suckling bouts terminated by the mother were considerably shorter than those the foal stopped itself [15], [20]. We found that pregnant mare allowed her foal to suck longer when it was her who determined the length of a suckling bout. While frequency of suckling did not change in relation to pregnancy it means pregnant mares did not restrict, but increased filling of foal's needs compared to non-pregnant herdmates.

It suggests that lactating pregnant mares enhanced maternal investment to a nursed foal during early stages of pregnancy. This is most likely because they expect increasing trade-off between investment to a nursed foal and a growing foetus later in pregnancy when demands of their foetus increase. Low initial demands of a foetus increase from mid-gestation and most of the foetal growth during the last trimester of pregnancy [26]; pregnancy in horses normally ranges between 315 to 365 days, with the average being about 340 days [27]. This increase seems to be well reflected by equid mares who wean their foals earlier than barren ones [6], [10], [11], [13] and time the weaning often just around forthcoming of the last trimester of pregnancy.

Pregnant mares can presumably start altering their maternal behaviour towards a nursed foal early after conception as the recognition of pregnancy by the mare's organism should occur on physiological basis between day 7 and day 17 (when the constant movement of the equine conceptus throughout the uterus ensures release of maternal recognition of pregnancy signal onto the endometrium in all parts of the uterus [28].

Thus pregnant mares may, through more intensive maternal care (relaxed mother-offspring conflict) during early stages of lactation, compensate their nursed foals for later decrease in investment due to increasing demands of the foetus and/or for the shorter period of milk supply. Barren mares, on the other side, are not under pressure of dual investment and wean their foals usually later so they can spread their maternal investment over a longer period of lactation. In our study weaning process could not be investigated as foals were artificially weaned before they reached 7 months of age, all of them earlier than spontaneous weaning occurred or the mothers reached last trimester of pregnancy. However, as milk production declines considerably by six months of lactation [29], our observations covered the period of most intensive milk provision. Further research is needed in this area.

We did not detect any effect of mother's pregnancy on foals' frequency of suckling solicitations or duration of suckling bout stopped by the foal on its own which does not suggest effort of the foals to compensate for increased mother-offspring conflict in pregnant mares.

Low rates of either foals' suckling attempts rejected (1%) or sucklings terminated (15%) by the mother in our study most likely resulted from optimal nutrition the mares were provided with. It presumably means the foals' needs were fulfilled as suggested also in Estep et al. (1993). Since pregnancy of the mother apparently altered suckling behaviour under these conditions indicating a low level of parent-offspring conflict it should be considered further when analyzing suckling behaviour in terms of maternal investment or mother-offspring conflict in free-living population of equids exhibiting usually high mother-offspring conflict.

The only study providing evidence about effect of pregnancy on suckling characteristics during period of milk provision in equids [15] revealed just opposite trends to ours; pregnant captive plains zebra mares kept in ZOO allowed shorter suckling bouts to a foal when they themselves determined a length of a suckling bout which indicated higher parent–offspring conflict in pregnant mares compared to non-pregnant ones. In spite of this, results of both studies may not be in conflict due to different period the foals were investigated. While plains zebras study covered phase of weaning conflict as most of the foals were observed until natural weaning which occurred in pregnant mares from 243 to 355 days of foal's age [15], [18], all of our foals were artificially weaned before they reached the age of 210 days, i.e., mostly earlier than weaning process could have even started. Thus both studies are not comparable in this aspect and detailed analyses of mother-offspring conflict during particular stages of pregnancy/lactation should be performed.

Nursing a foal during the first two trimesters of pregnancy had no negative impact on birth weight of the foetus. However, the effect of lactation in later stages of pregnancy should be address to further research.

To our knowledge, this is the first study showing a lower mother-offspring conflict in pregnant than in non-pregnant lactating females while expecting just the opposite. Our results suggest that pregnant mares cope with parallel investment into a nursed foal and a foetus through enhancing nursing behaviour in early stages of pregnancy before the initially low requirements of the foetus increase. They compensate their suckling foal with the perspective of its early weaning due to ongoing pregnancy. We expect such role of pregnancy not just in free-living populations of equids, but also in other ungulate species with dual maternal investment, e.g., in cattle, buffalo or goats.

Acknowledgments

We thank Adam Dušek and anonymous referees for their helpful comments on the manuscript and Jitka Komárková and Marta Komárková for their excellent field assistance. We highly appreciated help of Jan Kokoška who improved the English. We are grateful to Lenka Gotthardová, the former director of the National stud Kladruby nad Labem, for enabling realization of our project there, as well as for kind assistance of her and other stud staff, mainly Illona Křížová.