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Diurnal nursing pattern of wild-type European rabbits under natural breeding conditions

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  • Université Sorbonne Paris Nord

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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. ...
Article
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.
... 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). ...
Article
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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. ...
Article
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. ...
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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.
... Several studies, performed on domestic rabbit breeds -kept under laboratory or farm conditions (Coureaud et al., 2000;Deutsch, 1957;González-Mariscal, Mc Nitt, & Lukefahr, 2007;Lincoln, 1974;Venge, 1963;Zarrow, Denenberg, & Anderson, 1965)-or on wild rabbits kept in outdoor enclosures (Hoy & Selzer, 2002;Rödel et al., 2012), plus observations of wild rabbits in nature (Broekhuizen, Bouman, & Went, 1986;Broekhuizen & Mulder, 1983) have repeatedly confirmed that most does nurse the litter only once per day. ...
Article
locomotion, body temperature, blood and intraocular pressure, corticosteroid secretion, and sleep. Control of several circadian rhythms involves a light‐entrained circadian clock and a food‐entrained oscillator. Nursing periodicity, however, relies on a suckling stimulation threshold. Brain structures regulating this activity include the paraventricular nucleus and preoptic area, as determined by lesions and quantification of cFOS‐ and PER1 clock gene‐immunoreactive proteins. Melatonin synthesis in the rabbit pineal gland shows a diurnal rhythm, with highest values at night and lowest ones during the day. In kits the main zeitgeber is milk intake, which synchronizes locomotor activity, body temperature, and corticosterone secretion. Brain regions involved in these effects include the median preoptic nucleus and several olfactory structures. As models for particular human illnesses rabbits have been valuable for studying glaucoma and cardiovascular disease. Circadian variations in intraocular pressure (main risk factor for glaucoma) have been found, with highest values at night, which depend on sympathetic innervation. Rabbits fed a high fat diet develop cholesterol plaques and high blood pressure, as do humans, and such increased fat intake directly modulates cardiovascular homeostasis and circadian patterns, independently of white adipose tissue accumulation. Rabbits have also been useful to investigate the characteristics of sleep across the day and its modulation by infections, cytokines and other endogenous humoral factors. Rabbit circadian biology warrants deeper investigation of the role of the suprachiasmatic nucleus in regulating most behavioral and physiological rhythms described above. This article is protected by copyright. All rights reserved.
... An adequate microclimate in the nest box is essential for the kits (Mahmoud and Tulip, 2004), as hypothermia is the second highest frequent cause of death (17%) during the postnatal period (Rossel, 2005). European wild rabbit does (Oryctolagus cuniculus) leave their kits alone after kindling and after the brief daily nursings (Hudson and Distel, 1982;Rödel et al., 2012;González-Mariscal et al., 2013). Therefore, the entrance of the hole is closed by does suddenly after parturition in nature (Deutsch, 1957;Lloyd and McCowan, 1968;Hudson and Distel, 1982;Broekhuizen and Mulder, 1983). ...
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Nest quality is important for the survival of new-born rabbits. Nesting material in rabbit farms generally consists of wood shavings, which is completely different from the dry grass used by the European wild rabbit ( Oryctolagus cuniculus ). The aim of the experiments was to examine which nest materials are preferred by rabbit does when building their nest. In experiment 1, the choice of multiparous rabbit does (n=37) among nest boxes bedded with different nesting materials was monitored. In each pen (1.0×1.83 m) 1 doe and 4 nest boxes (0.37×0.23×0.31 m) with different nest materials (meadow hay [H], wheat straw [S], fine fibre material [Lignocel<sup>®</sup>, L] or wood shavings [W]) were placed 3 days before the expected parturition (gestation length is about 31 d in the Pannon White breed). Some 48.6% of the does kindled in nest boxes that contained pure materials (L: 40.5%, S: 5.4%, H: 2.7%), and 51.3% of the does kindled in nest boxes where the nest materials of different nest boxes were mixed by the does (S with L: 21.5%, S with L and H: 5.4%, W with L: 8.1%, L with H and S: 5.4%). Does preferred kindling in the nest box bedded with L, and most of them refused the nest box with W. In experiment 2/a (n=32 does) and 2/b (n=25 does), each pen (1×0.91 m) was equipped with 3 and 2 hay racks and filled with H, S or L, and H or S, respectively. The experiments lasted from the 27<sup>th</sup> day of pregnancy until the day of parturition and 24-h video recordings (10 does/experiment) were evaluated throughout the experiment. The events of carrying the nest materials from the hay racks were registered. In experiment 2/a, the frequency of nest material carrying was highest on the day of parturition. The preferred nest material was L (compared to H and S) on each experimental day except day 30 of pregnancy. At the day of kindling, 87.5, 6.3 and 6.3% of the nests contained pure L, mixed L-H and L-S, respectively. In experiment 2/b, the frequency of nest material carrying (mostly S) was highest on the day of parturition, and on days 27 and 30 of pregnancy. More does built nests with only S (72%) than H (16%), and in 12% of the cases the S and H were mixed. For the purpose of nest building, material S was the most frequently used (72%) compared to other possibilities (H: 16%, S-H: 12%). It can be concluded that rabbit does showed the following clear preferences for specific nest building materials: L>S>H>W.
... The altricial, naked young are born into a nest of grass and fur constructed by the mother in a nursery burrow (or laboratory nest box) [9,10]. Mothers leave the young almost immediately after giving birth and only return for a few minutes approximately once every 24 h to nurse [11][12][13][14]. At around postnatal days 18-20, under natural conditions, the young emerge from the nursery burrow and are typically weaned during the following 10 days [15,16]. ...
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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. In this study, we investigate the development of individual differences in chin‐marking behavior (chinning) in the domestic rabbit and relate this to individual differences in growth and behavior among littermates during the early postnatal period. Individual differences among litter siblings in the frequency of chinning remained stable across the postweaning period until sexual maturity. However, we found no significant associations between individual differences in chinning and individual differences in the morphological, physiological, or behavioral variables known to form a well‐correlated early developmental complex in this species.
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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.
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