Vocalizations as an indicator of pregnancy in local domestic rabbit does: preliminary study

I Ilès

Laboratory of Animal Health and Production, National Veterinary High School, Algiers, Algeria
iles_imene@yahoo.fr

Abstract

This research has studied the vocalizations of rabbit does exposed to buck in relation to their reproductive state (pregnant or not). A total of 107 nulliparous does (4.5-5 months old, weighing 3102±28 g) and 30 adult bucks (7-10 months old, weighing 3150±30 g) from a local population were used. During the vocalization test, each female was placed into the cage of the buck, and her vocal behavior was noted (vocalized or not) and recorded as variable of Bernoulli (0-1) on mating day (D0) and on day 12 after mating (D12). The results showed that at D0, only 2.8% of nulliparous does vocalized. At D12, the proportion of females which vocalized was significantly more important: 58.4±4.1% vs. 2.8±1.6% at D0 (p<0.001). On D12, the does vocalized more frequently when they were pregnant: 75.3±4.8% vs. 7.6±5.3% for pregnant and not-pregnant does respectively (p<0.001), and 96.8±2.2 % of females which vocalized on D12 were pregnant. This study showed that vocalizations of rabbit does, placed in contact with male on day 12 after mating, were significantly increased when the females were pregnant (+67.7%). The vocalization test could be used as a complementary indicator of pregnancy in domestic rabbits.

Key words: Algeria, behavior, pregnancy diagnosis, vocal communication

Les vocalisations comme indice de gestation chez la lapine domestique locale : étude préliminaire

Résumé

Cette recherche a étudié le comportement vocal des lapines placées au contact des mâles, en relation avec leur statut reproductif (en gestation ou non). Un effectif de 107 lapines nullipares (4,5 à 5 mois d’âge et d’un poids corporel moyen de 3102±28 g) et de 30 mâles adultes (7 à 10 mois d’âge et d’un poids moyen de 3150±30g), issu de la population locale, a été utilisé. Au cours du test de vocalisation, réalisé le jour de la saillie (J0) et le douzième jour après la saillie (J12), chaque femelle a été placée dans la cage du mâle, et son comportement vocal (vocalise ou non) a été noté comme une variable de Bernoulli (0-1). Les résultats ont montré qu’à J0, seulement 2,8% des femelles ont vocalisé. A J12, la proportion des femelles qui ont vocalisé a été significativement plus importante : 58,4±4,1% vs. 2,8±1,6% à J12 et à J0 respectivement (p<0,001). A J12, les femelles ont vocalisé plus fréquemment lorsqu’elles étaient en gestation (75,3±4,8% vs. 7,6±5,3%, respectivement chez les femelles en gestation ou non, p<0,001) et 96,8±2,2% des lapines qui ont émis des vocalises étaient en gestation. Cette étude a montré que les vocalisations des lapines, placées au contact des mâles 12 jours après la saillie, ont augmenté de façon significative lorsque les femelles étaient en gestation (+67,7%). Le test de vocalisation pourrait être utilisé comme un indice complémentaire de gestation chez la lapine domestique.

Mots-clés: Algérie, comportement, communication vocale, diagnostic de gestation

Introduction

In some mammals, evidence exists that the vocal behavior can contain information on the reproductive state. In heifers, several studies showed that the estrous climax results in an increase in vocalization rate (Schön et al 2007; Röttgen et al 2018). In the Norway rat ( Rattus norvegicus), vocalization is one of the most reliable characteristic of male copulatory behavior (Barfield et al 1979). Vocalization can also provide an index of the affective state of the animal, or, as in the case of farm animals, as a measure of welfare (Manteuffel et al 2004). Several factors can influence vocal behavior, such as external events or hormonal status. These factors are perceived by the limbic centers of the forebrain; the signals are then transferred via centers of the midbrain to effector muscles of the vocal system (Manteuffel et al 2004). Kiley (1972) showed that the activation of sympathico-adrenomedullary axis tends to increase the probability of vocalization. In pig, endocrine stress response, as adrenaline release, induce changing rates of specific type of vocalization (Marchant-Forde et al 2001). Rabbits have a variety of vocal communications; the content rabbits grind their teeth at a low volume, while extreme fright is demonstrated by a loud scream (Crowell-Davis et al 2007). In rabbits, the acoustic communications occurred in the beginning of the life. Shuh et al (2004) showed that the kits improve the number of their vocalizations during the hourly interval prior to nursing, and this behavior is described from birth up to the 14^th day of life. Otherwise, rabbit mother responds rapidly to pup distress calls (Rödel et al 2013).

The relationships between reproductive state and vocal behavior were rarely explored in rabbit females. Previous research described sporadic or continuous vocalizations in some pregnant does introduced into the male’s cage (Stoufflet et Caillol 1988). Pacs and Szabó (1990) noted that, if the does were pregnant, their vocal behavior changed towards the buck. For these authors, their vocalization, qualified as “weeping sound”, is one of the most evident signs of pregnancy in rabbits. To our knowledge, no experimental research has verified this hypothesis. Thus, our objective was to study the vocal behavior of rabbit does when they are placed in contact with male. The vocalizations rate was analyzed in relation to the physiological status of the female (pregnant or not).

Materials and methods

Animals housing

The trial was conducted in the experimental rabbitry of the National Veterinary School of Algiers. The mean ambient temperature recorded was 19.3±3.7°C, and the relative humidity 67.4±13.0%. The animals were reared in a naturally ventilated building, and maintained under natural light-dark photoperiod. A total of 107 nulliparous does (4.5-5 months old, weighing 3102±28g) and 30 adult bucks (7-10 months old, weighing 3150±30g) from a local rabbit population (Zerrouki et al 2005) were used. Males and females were housed in the same rabbitry. The females were kept in individual cages for reproductive does (46.5 x 62.0 x 29.0 cm height), formed by galvanized wire mesh. The rabbits were feed ad libitum with a commercial pellet (SARL “Production locale”, Bouzaréah, Algiers) and had free access to water, with nipple drinkers. The nulliparous does were mated naturally and the diagnosis of gestation was performed by abdominal palpation on day 12 after mating. The wooden nest-boxes were attached to the front side of the maternal cage 7 days before kindling.

Experimental design

The test was based on the observation of audible vocalization emitted by the female. For each female, the vocalization-test occurred at two times: on mating day (D0) and on day 12 postmating (D12). During the vocalization-test, the female was placed into the cage of the buck for approximately 3 minutes, in contact to the male. The test allowed the female to receive olfactory, visual and tactile stimulation from the buck. The vocal behavior of the doe was recorded as variable of Bernoulli (0-1): the observer heard call emitted by the doe (1); the observer did not hear any sound emitted by the doe (0).

For the vocalization-test on D12, the mating was not allowed: when the male attempted to mount the female, he was prevented by the observer. On D12, the vocalization-tests occurred immediately after pregnancy diagnosis by abdominal palpation. All the vocalization-tests were observed by the same person.

In the aim to evaluate the reproductive performance of the nulliparous does, the following parameters were recorded at kindling, for each of the litters: total litter size, number of kits born alive, weight of total kits born per litter, weight of kits born alive per litter.

In order to assess the emotional state of the rabbit does, their maternal behavior during the peripartum period was determined. For each parturition, five criteria related to maternal behavior were recorded:

• Nest-building: presence (or not) of maternal hair inside the nest box (González-Redondo et Zamora–Lozano 2008).
• Place of birth: all kits inside the nest box / some or all kits outside the nest box (González-Redondo et Zamora–Lozano 2008).
• Nursing: nursing (or not) during the 24 hours after kindling (Coureaud et al 2000).
• Neonatal cannibalism: defined as the doe’s consumption of all or part of the body of at least one neonate from her litter (Denenberg et al 1960).

Statistical analysis

The data were analyzed using Statistica software (version 6). Proportional data were recorded as variable of Bernoulli (vocalize=1, no vocalize=0; pregnant =1; not pregnant =0). Percentages of vocalizations on D0 and D12 were compared with a Student’s t-Test for paired samples. The relationship between does vocal behavior (vocalize or not) and pregnancy was tested using a Chi-square test. The results were presented as mean ± standard error of the mean (SEM), and considered significant at p<0.05.

Results

The results were based on 214 (107 x 2) observations. Reproductive performance of the nulliparous does are reported in Table 1. Average pregnancy rate recorded in our experimentation was 75.7 % (n=81). One female was dead on day 24 of pregnancy.

At D0, vocalizations were extremely rarely observed in nulliparous does placed in contact with the male. Only 2.8±1.6% (n=3) of females vocalized when placed into the male cage.

The proportion of females which vocalized on D12 (n=63) was significantly more important in comparison to D0 (58.8±4.1% vs. 2.8±1.6%, p<0.001). The results show a significant correlation between vocal behavior and physiological state of the female (p<0.001): the does exposed to the male vocalized more frequently when they were pregnant (75.3±4.8% vs. 7.6±5.3%, for pregnant and no-pregnant does respectively, p<0.001; Figure 1). Moreover, 96.8±2.2% of females which vocalized (n=63) were pregnant (Table 2). However, in the group which did not emit vocalizations (n=44), 45.4±4.0% were pregnant. In the majority of cases, the sound does not appear until the female was placed in contact with the buck. In rare cases, the pregnant female began to vocalize when we opened his cage and handled it. All rabbit females’ vocalizations observed during this study were very similar: they varied however in intensity. The does vocalized more intensively when the male tried to mount upon them. These vocalizations were like repetitive plaintive sounds.

Figure 1. Vocalizations rate in nulliparous rabbit does on day 12 after mating (%) (p<0.001)

Discussion

The reproductive performances recorded in the current trial were similar to those reported by Zerrouki et al (2005) for Algerian rabbit local population. Otherwise, the percentage of females who have built a nest or nursed their litters was consistent with that reported by the literature (Zarrow et al 1963; González-Redondo P et Zamora–Lozano M 2008).

Our results showed that audible vocalization rate was significantly increased in pregnant female in comparison to not pregnant. Pacs and Szabò (1990) studied the sexual ethology of New Zealand White and Californian rabbits, and observed that on days 8-10 after mating, pregnant female expressed specific sound when placed in contact with the buck. Our study confirms the observation of these authors. In the current study, the percentage of pregnant females that did not vocalize is quite high (45.4%). Previous works evidenced that there was no relationship between rabbit does vocal behavior and their sexual receptivity during pregnancy (Stoufflet et Caillol 1988) or during pseudopregnancy (Caillol et al 1983). The hormonal status during pregnancy could influence the vocal behavior. In rabbit, the plasma concentration of progesterone increased from day 3 until day 12-15 of pregnancy and declined slowly thereafter until term (Challis et al 1973).

The reason why pregnant rabbits exposed to male improve their vocalization is not clear. In pregnant rabbit, the mating is not able to induce ovulation (Mills et Gerardot 1984), thus superfetation is not observed in rabbit, in opposition to the hare (Lepus europaeus) (Caillol et Martinet, 1983). In rabbit, vocal communication –like growls– are occasionally used to express anger or annoyance (Bays et al 2006). Mating occurring during pregnancy could represent a discomfort or a stress for the doe. Previous observations reported that stress could modify vocalization rate. In pigs, a central injection of anxiogenic peptides (e.g., corticotropin releasing hormone) induced an increased vocalization rate (Parrott et al 2000). It has also been demonstrated that both cows and calves vocalized in response to separation (Marchant-Forde et al 2002). The vocalizations emitted by the pregnant rabbit could inform the male on his reproductive state. In the rat, the postejaculatory vocalizations emitted by the male signals a state of sexual incapacity; they served to maintain separation between male and female during the postejaculatory interval (Barfield et al 1979).

Our study showed that the vocalization-test could be used as a complementary indicator of pregnancy in domestic rabbits. However, further investigations are needed to define the utility of the vocalization test as a pregnancy diagnosis, and the advantages it offers compared to palpation, taking into consideration animal welfare. In rabbit, pregnancy is habitually diagnosed by an abdominal palpation on days 10-14 after insemination. The palpation technique is not effective if performed before the ninth day, while after day 14, there is an increased risk of abortion (Lebas et al 1997). Now, only the use of echography permits to have an earlier pregnancy-diagnosis in rabbit which embryo vesicles are visible on day 7-8 postcoïtum (Ypsilantis et Saratsis, 1999; Caron et al 2012).

Conclusions

• This research has shown that only 7.6% non-pregnant nulliparous rabbit does emitted audible vocalizations when putted into the cage of a male, in contact to the buck at D12.
• In contrast, pregnant nulliparous rabbit increased their vocal communication when placed in contact with male (+67.7%): 75.3±4.8 vocalized when pregnant at D12.
• The vocalization test could be used as a complementary indicator of pregnancy in domestic rabbits. Further works must define at which day of pregnancy began this specific vocal behavior, if it can be observed until the end of pregnancy, and his role or meaning in rabbit reproduction.

Acknowledgements

The author wishes to thank Miss Boukhari Salima for her technical assistance during the trial. This work was supported by the National Research Program (Ministry of Higher Education and Scientific Research, Algeria).

References

Barfield J R, Auerbach P, Geyer L A and McIntosh T K 1979 Ultrasonic vocalizations in rat sexual behavior. American Zoologist, 19, 469-480.

Bays B T, Lightfoot T and Mayer J 2006 Rabbit behavior. In: “Exotic Pet Behavior: Birds, Reptiles and Small Mammals”. 1st edition, Elsevier, St Louis, 1-49.

Caillol M and Martinet L 1983 Mating periods and fertility in the doe hare (Lepus europaeus) bred in captivity. Acta Zoologica Fennica, 174, 65-68.

Caillol M, Dauphin-Villemant C and Martinet L 1983 Estrus behavior and circulating progesterone and estrogen levels during pseudopregnancy in the domestic rabbit. Journal of Reproduction and Fertility, 69:179-186.

Caron M, Bencharif D, Briand L and Tainturier D 2012 Diagnosis and ultrasonic examination of pregnancy in the rabbit with a probe of 12.5 MHz. Revue de Médecine Vétérinaire, 163, 6, 309-315. http://www.revmedvet.com/artdes-us.php?id=15840

Challis J R, Davies J and Ryan K J 1973 The concentrations of progesterone, estrone and estradiol-17-β in the plasma of pregnant rabbits. Endocrinology, 93 (4), 971-976.

Coureaud G, Schaal B, Coudert P, Rideaud P, Fortun-Lamothe L, Hudson R and Orgeur P 2000 Immediate postnatal suckling in the rabbit: Its influence on pup survival and growth. Reproduction Nutrition Development, 40, 19-32.

Crowell-Davis S L 2007 Understanding rabbit behavior and preventing and treating behavior problems. Journal of Exotic Pet Medicine, 10, 38-44.

Denenberg V H, Petropolus S F, Sawin P B and Ross S 1960 Genetic, physiological and behavioural backround of reproduction in the rabbit: VI Maternal behavior with reference to scattered and cannibalized newborn and mortality. Behaviour,15, 71-76.

González-Redondo P and Zamora–Lozano M 2008 Neonatal cannibalism in cage-bred wild rabbits (Oryctolagus cuniculus). Archivos de Medicina Veterinaria, 40, 281-287.

Kiley M 1972 The vocalizations of ungulates, their causation and function. Zeitschrift für Tierpsychologie 31, 171-222.

Lebas F, Coudert P, de Rochambeau H and Thébault R G 1997 Rabbitry management. In: “The rabbit, husbandry, health and production. FAO Animal Production and Health”, Series n°21 chapter 7, 149-164. http://www.fao.org/docrep/t1690e/t1690e00.HTM

Manteuffel G, Puppe B and Schön P C 2004 Vocalization of farm animals as a measure of welfare. Applied Animal Behaviour Science, 88, 163–182.

Marchant-Forde J N, Whittaker X and Broom D M 2001 Vocalisations of the adult female domestic pig during a standard human approach test and their relationships with behavioural and heart rate measures. Applied Animal Behaviour Science 72, 23–39.

Marchant-Forde J N, Marchant-Forde R and Weary D M 2002 Reponses of dairy cows and calves to each other’s vocalisation after early separation. Applied of Animal Behavior Science, 78, 19–28.

Mills T M and Gerardot R J 1984 Dissociation of copulation from ovulation in pregnant rabbits. Biology of Reproduction, 30, 1243-1252.

Pacs I and Szabó L 1990 Sexual ethology of rabbits. In: “ Proceeding of the 3rd World Rabbit Congress”, Rome, Italy, 468-472.

Parrott R F, Vellucci S V and Goode J A 2000 Behavioral and hormonal effects of centrally injected “anxiogenic”neuropeptides in growing pigs. Pharmacology Biochemistry and Behavior, 65, 123–129.

Rödel H G, Landman C, Starkloff A, Kunc H P and Hudson R 2013 Absentee mothering-Not so absent ? Responses of European rabbit ( Oryctolagus cuniculus) mothers to pup distress calls. Ethology, 119, 1-10.

Röttgen V, Becker F, Tuschscherer A, Wrenzycki C, Düpjan S, Schön P C and Puppe B 2018 Vocalization as an indicator of estrus climax in Holstein heifers during natural estrus and superovulation. Journal of Dairy Science, 101 (3), 2383-2394. https://ac.els-cdn.com/S0022030218300092/1-s2.0-S0022030218300092-main.pdf?_tid=e39a2ab1-40ae-4a39-892d-33948d24b71a&acdnat=1520852178_c52a8b1d45f99470f010a34c5b593ad5

Schön P C, Hämel K, Puppe A, Tuchscherer A, Kanitz W and Manteuffel G 2007 Altered vocalization rate during the estrus cycle in dairy cattle. Journal of Dairy Science, 90, 202-206. www.researchgate.net/publication/6617513_Altered_Vocalization_Rate_During_the_Estrous_Cycle_in_Dairy_Cattle

Schuh D, Hoy S T and Selzer D 2004 Vocalization of rabbit pups in the mother-young relationship. In “Proceedings of the 8^th World Rabbit Congress”, September 7-10, 2004,Puebla, Mexico. http://world-rabbit-science.com/WRSA-Proceedings/Congress-2004-Puebla/Papers/Welfare%20&%20Ethology/W-Schuh.pdf

Stat Soft France 2003 Statistica (version 6). Logiciel. 31 cours des Juilliottes, 94 700 Maisons-Alfort, France.

Stoufflet C and Caillol M 1988 Relation between circulating sex steroid concentrations and sexual behaviour during pregnancy and postpartum in the domestic rabbit. Journal of Reproduction and Fertility, 82, 209-218.

Ypsilantis P and Saratsis P H 1999 Early pregnancy diagnosis in the rabbit by real time ultrasonography. World Rabbit Science, 7 (2), 95-99. https://polipapers.upv.es/index.php/wrs/article/view/385/372

Zarrow M X, Farooq A, Denenberg V H, Sawin P B and Ross S 1963 Maternal behavior in the rabbit: endocrine control of maternal nest-building. Journal of Reproduction and Fertility, 6, 375-383.

Zerrouki N, Bolet G, Berchiche M and Lebas F 2005 Evaluation of breeding performance of a local Algerian rabbit population raised in the Tizi-Ouzou area (Kabylia). World Rabbit Science, 13, 29–37. https://polipapers.upv.es/index.php/wrs/article/view/531/0

Received 12 March 2018; Accepted 8 April 2018; Published 1 May 2018

Go to top