ABSTRACT

The European rabbit Oryctolagus cuniculus has an unusual pattern of nursing behavior. After giving birth in a nursery burrow (or laboratory nest box), the mother immediately leaves the young and only returns to nurse for a few minutes once approximately every 24 h. It has been assumed this schedule, like a variety of other functions in the rabbit, is under circadian control. This assumption has been largely based on findings from mothers only permitted restricted access to their young once every 24 h. However, in nature and in the laboratory, mothers with free access to young show nursing visits with a periodicity shorter than 24 h, that does not correspond to other behavioral and physiological rhythms entrained to the prevailing 24 h light/dark (LD) cycle. To investigate how this unusual, apparently non-circadian pattern might be regulated, we conducted two experiments using female Dutch-belted rabbits housed individually in cages designed to automatically register feeding activity and nest box visits. In Experiment 1 we recorded the behavior of 17 mothers with free access to their young under five different LD cycles with long photo and short scotoperiods, spanning the limits of entrainment of the rabbit’s circadian system. Whereas feeding rhythms were entrained by LD cycles within the rabbit’s circadian range of entrainment, nursing visits showed a consistently shorter periodicity regardless of the LD regimen, largely independent of the circadian system. In Experiment 2 we tested further 12 mothers under more conventional LD 16:8 cycles but “trained” by having access to the nest box restricted to 1 h at the same time each day for the first 7 d of nursing. Mothers were then allowed free access either when their young were left in the box (n = 6), or when the litter had been permanently removed (n = 6). Mothers with pups still present returned to nurse them on the following days according to a similarly advancing pattern to the mothers of Experiment 1 despite the previous 7 d of “training” to an experimentally enforced 24 h nursing schedule as commonly used in previous studies of rabbit maternal behavior. Mothers whose pups had been removed entered the box repeatedly several times on the first day of unrestricted access, but on subsequent days did so only rarely, and at times of day apparently unrelated to the previously scheduled access. We conclude that the pattern of the rabbit’s once-daily nursing visits has a periodicity largely independent of the circadian system, and that this is reset at each nursing. When nursing fails to occur nest box visits cease abruptly, with mothers making few or no subsequent visits. Together, these findings suggest that the rabbit’s once-daily pattern of nursing is regulated by an hourglass-type process with a period less than 24 h that is reset at each nursing, rather than by a circadian oscillator. Such a mechanism might be particularly adaptive for rhythms of short duration that should end abruptly with a sudden change in context such as death or weaning of the young.

摘要

欧洲兔穴孔兔有异常的护理行为模式。母亲在苗圃洞穴（或实验室巢箱）中分娩后，母亲立即离开了年轻人，仅大约每24小时一次回到护士那里几分钟。像兔子的其他各种功能一样，已经假定该时间表是在昼夜节律的控制之下。这个假设主要是基于母亲的发现，母亲每24小时只允许一次限制接触年轻的孩子。但是，在自然界和实验室中，母亲可以自由地接受年轻护理，其护理周期少于24小时，这与流行的24小时明/暗（LD）周期所带来的其他行为和生理节律不符。为了研究如何调节这种异常的，显然是非昼夜节律的模式，我们使用单独放置在笼子中的荷兰带状雌性兔进行了两个实验，这些笼子设计用于自动记录饲养活动和巢箱访问。在实验1中，我们记录了17名准妈妈在五个不同的LD周期内可以自由接触自己的幼仔的行为，包括长照和短短脚目，跨越了兔子昼夜节律系统的限制。尽管在兔子的昼夜节律范围内，LD周期会诱使进食节律，但无论LD方案如何，护理访视均显示出持续较短的周期，这在很大程度上与昼夜节律系统无关。在实验2中，我们在更常规的LD 16：8周期下测试了另外12名母亲，但在最初的7天护理中，每天每天同一时间限制进入巢箱1小时，从而“接受了训练”。n = 6），或永久性清除了垃圾（n= 6）。仍然有幼崽的母亲在第二天按照与实验1的母亲相似的方式返回给她们喂奶，尽管先前的7天“训练”到实验性的24小时护理时间表，这在以前的兔子研究中是常用的产妇的行为。在没有限制的第一天，被取走幼崽的母亲多次进入箱子，但是在随后的日子里，这种情况很少发生，而且在一天中的时间显然与先前安排的访问无关。我们得出的结论是，兔子每天一次的护理就诊的模式具有很大程度上独立于昼夜节律系统的周期性，并且在每次护理时都会重置这种周期性。如果没有进行护理，产妇的巢箱就诊会突然停止，而母亲很少或没有进行后续诊治。一起，这些发现表明，兔子的每日护理方式是由沙漏型过程控制的，周期小于24小时（在每次护理时重置），而不是由昼夜节律振荡。这种机制可能特别适合短时节律，短时节律应突然终止，例如突然死亡或断奶。