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Diurnal nursing pattern of wild-type European rabbits under natural breeding conditions
Abstract and Figures
The European rabbit Oryctolagus cuniculus is an important model system in the study of mammalian
maternal behavior. This is at least partly due to the rabbit’s unusually limited pattern of maternal care,
characterized by the mother briefly visiting the young to nurse just once approximately every 24 h. In
studies of domestic breeds under laboratory conditions it has been found that females show a rather
predictable interval between these once-daily visits. However, as there are reports of considerable interindividual variation, the aim of our study was to identify factors with the potential to modify the rabbit’s
diurnal pattern of nursing, such as characteristics of the mother, litter size and also potential changes in
the nursing interval length during the early postnatal period.Westudied the time course of nursing visits
in wild-type rabbits in the natural setting of a large field enclosure in order to obtain results unbiased
by laboratory artifacts. Using an automatic portable gas analyzer, we monitored the timing of nursing
events by recording the change in oxygen concentration within natural breeding burrows occurring when
mothers entered to nurse and calculated the interval length between successive nursing events. During
the first nine postpartum days, when our study was conducted, rabbit mothers on average showed a
nursing interval of about 24 h. Return intervals remained rather constant in mothers of larger litters but
decreased in mothers with smaller litters, resulting in them visiting their young to nurse a little earlier
each night. Mothers’ age, day length and season did not affect nursing intervals. In conclusion, our study
confirms that under natural conditions rabbits nurse their young only once approximately every 24 h,
but that this pattern is not completely fixed and can be modulated by litter size, possibly via the strength
of sucking stimulation received by the mother during nursing.
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... In the European rabbit (Oryctolagus cuniculus), including its domesticated (laboratory) form, the altricial young are born into a nest of dry grass and fur constructed by the mother in a nursery burrow (or laboratory nest box). Immediately after giving birth the mother leaves the young and only returns for a few minutes approximately once every 24 h to nurse (Deutsch 1957;Hudson and Distel 1982;Broekhuizen et al. 1986;Hudson et al. 1999;Rödel et al. 2012;Zarrow et al. 1965;reviews in Hudson and Distel 1989;Jilge and Hudson 2001). This continues until the young, under naturalistic conditions, are abruptly weaned by the mother, usually around 1 month of age (Hudson et al. 1996;Lincoln 1974). ...
... In fact, there are at least two reasons to question the assumption of circadian control of the rabbit's daily pattern of nursing. First, both in the laboratory (Hudson et al. 1995;Jilge 1995) and nature (Rödel et al. 2012;review in Hudson and Distel 1989), rabbits with free access to their young usually return to the nest to nurse them somewhat earlier each day, at least during the first 1 to 2 weeks of lactation. As parturition usually takes place during the dawn or early daylight hours (Hudson et al. 1995(Hudson et al. , 1999reviews in Hudson and Distel 1989;Ninomiya-Alarcón et al. 2004), this results in the mothers' nursing visits advancing steadily back into the night (Hudson and Distel 1989;Hudson et al. 1995;Rödel et al. 2012). ...
... First, both in the laboratory (Hudson et al. 1995;Jilge 1995) and nature (Rödel et al. 2012;review in Hudson and Distel 1989), rabbits with free access to their young usually return to the nest to nurse them somewhat earlier each day, at least during the first 1 to 2 weeks of lactation. As parturition usually takes place during the dawn or early daylight hours (Hudson et al. 1995(Hudson et al. , 1999reviews in Hudson and Distel 1989;Ninomiya-Alarcón et al. 2004), this results in the mothers' nursing visits advancing steadily back into the night (Hudson and Distel 1989;Hudson et al. 1995;Rödel et al. 2012). The second reason is that if the nursing mother is pregnant with another litter as a result of postpartum mating (review in Martínez-Gómez et al. 2004), she will resist nursing at the experimentally scheduled time during the daylight hours, and if forced to do so, may have difficulty giving birth to the second litter. ...
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.
... Several studies have documented that in various domestic breeds, kept under a controlled photoperiod and a constant food supply, nursing occurs with a frequency approximating once/day in most does (Drewett et al. 1982;Lincoln 1974;Matics et al. 2004). If kept in outdoor enclosures, domestic strains and wild rabbit does also nurse at a frequency of approximately once/24 h, with most nursing episodes occurring during darkness (Hoy and Selzer 2002;Rödel et al. 2012). Such a reliable, predictable nursing periodicity relies on numerous factors of control that are only beginning to be unveiled. ...
... Smaller litters (i.e., 4 kits or less) lead to several entrances of the doe into the nest box across the day and, eventually, to a loss of maternal behavior (González-Mariscal et al. 2013a). Interestingly, wild rabbit does kept within an enclosure also show several entrances into the nursing burrow if they nurse small litters (Rödel et al. 2012). ...
Direct care of offspring by the father (sire) is relatively rare in primates. Besides humans, there are a number of species where the male is essential for the survival of offspring: marmosets, tamarins, titis and owl monkeys, some lemurs, and siamangs. All these species show reduced sexual dimorphism, territoriality, and biparental care. However, timing and levels of direct care may vary among these species. Here, relying on both lab and field data, we address the variability found in father's involvement with his infants, the behavioral, neuroendocrine and sensory systems that are a cause and consequence of paternal care, and social bonds between the breeding pair. We integrate studies of laboratory animals (where detailed observations and experimentation are possible) with field studies (which illuminate the ecological and evolutionary functions of paternal care) and discuss the future directions for examining the proximate and ultimate mechanisms of paternal care in nonhuman primates.
... In this temperature-controlled room, white light was on for 24 h a day to allow the video recording of the litters during the day and night (see 2.2.1.). Note that 2-to 4-day-old rabbit pups, as were used in our study, still have their eyes closed (eye opening at around postnatal day 10 [11,18]), and under natural conditions, pups of this species do not experience any notable changes in daylight in their nests situated inside the nursery burrow closed by the mother [46,47]. ...
Individual-level sibling interactions in the litter huddle have been studied extensively, especially in the domestic rabbit (Oryctolagus cuniculus). However, little is known about inter-litter differences in pup activity patterns during early postnatal life, in particular regarding the drivers of such variation. In our study on 2-3-day-old rabbit pups, we predicted lower locomotor activity in litters with lower mean body masses on the day of birth (starting body mass) and with lower daily milk intake per pup, possibly constituting a behavioral strategy of pups to cope with associated energetic constraints. For an automatized assessment of pup locomotor activity in the litter huddle, we successfully developed and validated a method based on the quantification of dissimilarities between consecutive frames of video footage. Using this method, we could confirm a U-shaped time course of litter-level locomotor activity, with maximum values shortly before and after the once-daily nursing typical for the rabbit. As predicted, between-litter variation in mean starting body mass and in daily milk intake affected the degree of locomotor activity in the litter huddle, in an interactive way. That is, in litters with heavier starting body masses, pup locomotor activity was greater in pups with an initially higher milk intake, suggesting that only pups with better body condition and a higher energy intake could afford higher levels of activity. This interaction was exclusively apparent during the middle phase of the 24-h inter-nursing interval, when litter activity was low. Shortly before nursing, when pups show higher levels of locomotor behavior in anticipation of the mother's arrival, and shortly after nursing when the pups were more active possibly due to adjustments of their positions in the huddle, activity levels were decoupled from pups' starting body mass and previous milk intake. Our findings highlight the importance of pup body mass and daily energy intake, two parameters known to be related to maternal characteristics, in shaping inter-litter differences in pup locomotor activity.
... This temperature, below the approximately 35°C critical thermo-neutral temperature for newborn rabbits (Hull, 1965;Pacheco-Cobos et al., 2003;Satinoff et al., 1976), induces them to huddle but without compromising pup survival (Bautista et al., 2003). In nature, the ambient temperature surround- Rödel et al., 2012;Zarrow et al., 1965). Immediately after the mother jumped out of the box, indicating the end of nursing, we weighed the pups individually and placed them back in the box inside the hoop, and placed the box under the acrylic cover. ...
Individual differences in behavior (“personality”) are of considerable interest to behavioral biologists. Important questions include how early in life such differences emerge, what factors influence their emergence, and whether they remain stable across development and into adult life. Given the demanding nature of longitudinal studies, there is a lack of information regarding these questions in mammals. Our aim in this study was to investigate the development of individual differences in chin‐marking behavior (chinning) in the domestic rabbit, a notable part of this species’ system of chemical communication, and to relate this to individual differences in growth and behavior among littermates during the early postnatal period. We tested repeatedly the frequency of chinning movements from weaning to sexual maturity in 63 chinchilla‐strain rabbits (35 females, 28 males) from 14 litters. Within litters, we found significant consistencies over time in this behavior, that is, in both sexes inter‐individual differences among litter siblings in the frequency of chinning movements remained stable across the postweaning period until sexual maturity. Unexpectedly, however, we found no significant associations with the morphological, physiological, or behavioral variables known to form a well‐correlated early developmental complex in this species. We tentatively conclude that in the rabbit, individual differences in the frequency of chinning have little relation to other previously studied aspects of individual developmental trajectories. The origin and functional significance of individual differences in chinning frequency, whether in reproductive or other social contexts is largely unknown and requires further investigation.
... The resulting within-litter variation in birth mass can lead to a cascade of effects reinforcing such differences via sibling interactions; this has been intensively studied in the European rabbit both in animals of wild origin and in its domestic form (Hudson et al. 2011;Rödel et al. 2017). As rabbit mothers do not brood their altricial young and only visit the nest once a day to nurse them briefly (Zarrow et al. 1965;Rödel et al. 2012), huddling among littermates is of paramount importance to save energy necessary for growth and survival (Bautista et al. 2003;Gilbert et al. 2007;Rödel et al. 2008b). Heavier pups are more successful in occupying more central and energetically more advantageous positions in the litter huddle than their lighter siblings and thus are able to maintain higher body temperatures and to convert milk into biomass more efficiently, all of which contribute to higher growth rates at least until around weaning (Rödel et al. 2008a;Bautista et al. 2015b;Zepeda et al. 2019). ...
Although littermates in altricial mammals usually experience highly similar environmental conditions during early life, considerable differences in growth and health can emerge among them. In a study on subadults of a European rabbit (Oryctolagus cuniculus) population with low MHC polymorphism, we tested whether litter-sibling differences in endoparasitic coccidia load and body mass at the end of the vegetation period were associated with within-litter differences in starting body mass (measured around 2 weeks prior to weaning) and in immune-genetic (MHC class II DRB) constitution. We hypothesized that siblings with a lighter starting mass might be more susceptible to endoparasite infections and thus, negative effects of a more unfavourable MHC constitution might be particularly pronounced in such individuals. Within-litter comparisons revealed that animals with a lighter starting mass reached a relatively lower body mass in autumn. Furthermore, there were indications for an allele-specific heterozygote advantage, as animals with heterozygous combinations of the allele Orcu-DRB*4 had relatively lower hepatic coccidia loads than their littermates with certain homozygous allele combinations. Consistent with our hypothesis, significantly higher hepatic coccidia loads and tendentially lower autumn body masses in homozygous compared to heterozygous individuals for the allele Orcu-DRB*4 were evident in initially lighter but not in heavier siblings, suggesting synergistic effects between an unfavourable MHC constitution and a light starting mass. Taken together, these effects might lead to notable differences in fitness among litter siblings, as a low body mass and a high endoparasite burden are key factors limiting young rabbits' survival during winter.
... fish: Clark et al., 2013, Payne et al., 2015aquatic turtles: Enstipp et al., 2011). With the advent of smaller electronic components, open-flow respirometry has also increasingly been taken to the field, to investigate energy budgets on free-ranging animals, often using natural sleeping sites (burrows, tree hollows, nest boxes) as metabolic chambers (Bartholomew and Lighton, 1986;Arnold et al., 1991;Lighton, 1996;Lighton and Duncan, 2002;Dausmann et al., 2009;Pretzlaff et al., 2010;Rödel et al., 2012;Berg et al., 2017;Langer et al., 2018;Reher et al., 2018). Free-ranging animals are usually exposed to a range of ambient temperatures; however, insulation of nests allows animals to establish a comparatively stable microclimate that can deviate quite substantially from ambient conditions (e.g. ...
Open-flow respirometry is a common method to measure oxygen-uptake as a proxy of energy expenditure of organisms in real-time. Although most often used in the laboratory it has seen increasing application under field conditions. Air is drawn or pushed through a metabolic chamber or the nest with the animal, and the O2 depletion and/or CO2 accumulation in the air is analysed to calculate metabolic rate and energy expenditure. Under field conditions, animals are often measured within the microclimate of their nest and in contrast to laboratory work, the temperature of the air entering the nest cannot be controlled. Thus, the aim of our study was to determine the explanatory power of respirometry in a set-up mimicking field conditions. We measured O2 consumption of 14 laboratory mice (Mus musculus) using three different flow rates [50 L*h⁻¹ (834 mL*h⁻¹), 60 L*h⁻¹ (1000 mL*h⁻¹) and 70 L*h⁻¹ (1167 mL*h⁻¹)] and two different temperatures of the inflowing air; either the same as the temperature inside the metabolic chamber (no temperature differential; 20 °C), or cooler (temperature differential of 10 °C). Our results show that the energy expenditure of the mice did not change significantly in relation to a cooler airflow, nor was it affected by different flow rates, despite a slight, but significant decrease of about 1.5 °C in chamber temperature with the cooler airflow. Our study emphasises the validity of the results obtained by open-flow respirometry when investigating energy budgets and physiological responses of animals to ambient conditions. Nevertheless, subtle changes in chamber temperature in response to changes in the temperature and flow rate of the air pulled or pushed through the system were detectable. Thus, constant airflow during open-flow respirometry and consequent changes in nest/chamber temperature should be measured.
... Yet, such a pattern is likely to be similar for other altricial, polytocous species also. Although it might be argued that such a pattern might be specific to the European rabbit given this species' system of "absentee" maternal care (see Broekhuizen et al. 1986;Rödel et al. 2012 for confirmation under natural or quasi-conditions), this might not be as unusual or extreme as it first appears. Studies based on laboratory or captive animals may overestimate the time mothers spend with their young, both because of limited cage space and lack of opportunity for mothers to distance themselves from their young, and the often ad libitum provision of food and water. ...
In altricial, litter-bearing species, huddling together with siblings during early life is a vital strategy to maintain a sufficiently high and stable body temperature. In this context, individual differences in huddling behavior within litters have been emphasized, as pups regularly occupying more central positions have relatively higher body temperatures, have quicker access to the mother’s nipples during nursing, and consequently show greater growth. However, it is not known whether such positive effects of a central litter huddle position on within-litter differences in growth translate into an overall higher weaning mass, taking into account strong contributors to among-litter growth variation, such as litter size and maternal parity. We used path analysis to investigate causal relations among these variables, based on data from 150 domestic rabbit pups from 24 litters. Our results confirmed positive, indirect effects of pups’ central litter huddle position on within-litter differences in early growth. This positive effect of a central litter huddle position also contributed to explaining a significant part of the overall across-litter variance in weaning body mass, apparent even when controlling for the direct negative effect of litter size, the direct positive effects of birth mass, and the lower offspring growth in primiparous compared to multiparous mothers. Thus, the results underline the key role of individual differences in litter huddle position in shaping within-litter but also overall variation in early growth. This might constitute an important mechanism accounting for how the positive association between body mass at birth and early growth is mediated in altricial, polytocous mammals.
Significance statement
Huddling together with siblings during early life saves energy and thus can contribute to early growth in small, altricial mammals. However, this strategy can also lead to individual differences within the litter, as heavier pups typically occupy energetically more favorable positions in the center of the huddle. In our study, we show and compare the different causal pathways underlying this effect. Most importantly, our analysis shows that advantages in early growth arising from a more central position in the litter huddle are also apparent when comparing pups across all litters—even though there is typically a notable variation in growth among different litters, for example due to litter size and maternal (parity) effects. In conclusion, the results underline the key role of sibling interactions within the litter in shaping differences in early growth, with potential fitness consequences during later life.
Rabbit maternal behavior (MB) impacts meat and fur production on the farm, survival of the species in the wild, and pet welfare. Specific characteristics of rabbit MB (i.e., three-step nest building process; single, brief, daily nursing bout) have been used as models for exploring particular themes in neuroscience, like obsessive-compulsive actions, circadian rhythms, and cognition. Particular hormonal combinations regulate nest building by acting on brain regions controlling MB in other mammals. Nonhormonal factors like type of lodging and the doe's social rank influence nursing and milk production. The concurrency of pregnancy and lactation, the display of nonselective nursing, and the rapid growth of altricial young - despite a minimal effort of maternal care - have prompted the study of mother-young affiliation, neurodevelopment, and weaning. Neurohormonal mechanisms, common to other mammals, plus additional strategies (perhaps unique to rabbits) allow the efficient, adaptive display of MB in multiple settings.
The European rabbit Oryctolagus cuniculus, ancestor of all domestic breeds, has an unusual pattern of maternal care in which females briefly nurse their young just once approximately every 24 h, and where the pups anticipate and prepare for their mother’s arrival. Chronobiologists have seen this as a model mammalian system to study the physiological and neurobiological underpinnings of a biologically relevant circadian complex. However, observations of nursing in wild rabbits, together with studies of nursing in domestic breeds allowed free access to their young in laboratory settings, suggest that the rabbit’s pattern of daily nursing visits resembles an hourglass rather than a circadian process, well suited to the sudden starts and stops of natural nursing cycles. We consider whether there might be other such cases in the literature, including in human chronobiology, in which failing to consider the organism’s natural, evolved daily patterns of behaviour and prematurely studying these under artificially imposed laboratory time schedules might have also led to such patterns being erroneously considered circadian.
The Amami rabbit Pentalagus furnessi is an endangered leporid species and is endemic to the two subtropical islands (Amami-Oshima Island and Tokunoshima Island) in the Ryukyu Archipelago in southwestern Japan. In total, 11 breeding burrows of this rabbit were detected from 1994 to 2017 in Amami-Oshima Island. Breeding was observed from November to December in most cases and in May in one case. The litter size was one in most cases, except for one burrow which had two offspring. Two burrows were observed during the entire delivery and nursing period for two different years, and the duration of breeding (from estimated date of delivery to the date when the offspring leaves the burrow) in these two burrows was 38 and 43 days. The mother visited the burrow periodically on alternate nights, and the duration of maternal visit was relatively short. The time at which the mother visited the burrow became progressively earlier in the night as the offspring became older. Although some aspects of breeding behaviour are similar to those of other lagomorphs, the Amami rabbit has an extremely small litter size with few breeding seasons in a year, resulting in the lowest fecundity rate among the lagomorph species. This unique reproductive trait is considered to have evolved in the small subtropical island environment that has a relatively stable climate with no native carnivorous mammals.
Maternal care in the European rabbit is limited to one brief nursing visit a day. To investigate the nature of this unusual mother- young relationship, four domestic does and their litters were kept separately except for the once-daily nursing, and the following parameters were recorded; from post-natal days 1 to 30, the duration of nursing bouts, daily milk yield, deposition of faecal pellets in the nest by does. daily weight gain of pups, eating of faecal pellets and nest material by pups, their water intake, and from post weaning days 31 to 44, their weight gain. Does were mated immediately after giving birth, and the measures for the first litters raised when does were pregnant were compared with the results for the second litters raised when does were not pregnant. Four control does and their litters were treated in the same way but without separating mothers and young. Pups progressed from drinking milk alone, to nibbling faecal pellets, to ingesting nest material, drinking water and finally to eating lab food. However, growth rates and the pattern of weaning depended on does' reproductive state. The first litters, raised by pregnant does, were significantly lighter and were weaned earlier than the second litters raised by the same does when not pregnant. The rabbit thus provides a particularly good opportunity to investigate the processes underlying the transition to independent feeding in a mammalian species.
Rabbits nurse briefly only once each night and are frequently both pregnant and lactating. To investigate the influence of the daily timing of nursing on parturition, does (n = 10 per group) were remated after giving birth and were allowed to nurse under one of three schedules: group 1 every 24 h in the light, group 2 every 24 h in the dark, and group 3 at any time. Whereas does from groups 2 and 3 nursed and gave birth normally, does of group 1, forced to nurse out of phase with the normal schedule, showed disturbed nursing behavior and prolonged gestation followed by many stillbirths. In a second experiment, pregnant does (n = 10 per group) were treated daily either with oxytocin (OT) in the light (group 4), with OT in the dark (group 5), or with progesterone (P; group 6) or saline (group 7) in the light. All does gave birth normally except those of group 4, which responded similarly to group 1 does. These findings demonstrate that in the rabbit, parturition may be seriously compromised if does nurse out of phase with the normal schedule and suggest that a shift in the daily timing of OT release may underlie this.
The main differences in nursing behaviour between Lepus and Oryctolagus cuniculus concern the period during which young rabbits stay in stopped breeding burrows; after emerging rabbit behaviour is very similar to that in hares.-from Authors
Continuous observations during three separate 24-hour periods were carried
out in late spring on a population of individually marked wild rabbits, Oryctolagus
cuniculus (L.), established in an artificially illuminated enclosure. Rabbits were
observed to feed throughout the night, with a peak at 2100 hr. Sexual behaviour
during post-parturn oestrus, and copulation between a buck and a virgin doe, are
described. An account of the daily activities of individual rabbits is given; and
the bearing of the observed pattern of activity on the reliability of sight counts
for the estimation of rabbit populations is discussed.