Levels of testosterone, progesterone and oestradiol in pregnant-lactating does in relation to aggression during group housing
DOI:
https://doi.org/10.4995/wrs.2021.14897Keywords:
rabbits, agonistic interactions, progesterone, testosterone, oestradiolAbstract
The neuroendocrine regulation of rabbit maternal behaviour has been explored in detail. However, little is yet known about the hormonal regulation of aggression in concurrently pregnant-lactating does, a reproductive condition that prevails during group housing of rabbits on farms. Therefore, in this study we determined the relation between a) the levels of progesterone, testosterone, and oestradiol during lactation; b) the anogenital distance at artificial insemination; and c) the timing of grouping with the intensity of agonistic behaviour, published previously. We performed four consecutive trials, where three groups of eight does each were artificially inseminated on day 10 postpartum (pp) and grouped on either day 12, 18 or 22 pp. Using Dipetalogaster maxima, a reduviid blood-sucking bug, we collected blood samples during the pregnant-lactating phase (days 13, 15, 17, 19, 21, 23 pp) on one or two randomly chosen does per treatment group. Testosterone levels varied little across the pregnant-lactating phase, agreeing with results from pregnant-only rabbits, while progesterone levels increased from day 3 (=13 dpp) to day 7 (=17 dpp) and remained unchanged until day 13 (=23 dpp) of pregnancy. All oestradiol concentrations fell below the limit of detection. Overall, all concentrations were slightly lower in comparison to rabbit studies with pregnantonly does. The agonistic behaviour was not related to the respective hormonal concentrations at grouping. In conclusion, the time point of grouping does after artificial insemination (AI) in the semi-group housing system only had a weak influence on aggression and the hormonal profile did not indicate an optimum time for grouping.
Downloads
References
Aguilar-Roblero R., González-Mariscal G. 2020. Behavioral, neuroendocrine and physiological indicators of the circadian biology of male and female rabbits. Eur. J. Neurosci., 51: 429-453. https://doi.org/10.1111/ejn.14265
Albert D.J., Jonik R.H., Walsh M.L. 1990. Hormone-Dependent Aggression in Female Rats: Testosterone Implants Attenuate the Decline in Aggression Following Ovariectomy I. Physiol. Behav., 47, 659-664. https://doi.org/10.1016/0031-9384(90)90074-E
Andrist C.A., Bigler L.M., Würbel H., Roth B.A. 2012. Effects of group stability on aggression, stress and injuries in breeding rabbits. Appl. Anim. Behav. Sci., 142: 182-188. https://doi.org/10.1016/j.applanim.2012.10.017
Andrist C.A., van den Borne B.H.P., Bigler L.M., Buchwalder T., Roth B.A. 2013. Epidemiologic survey in Swiss group-housed breeding rabbits: Extent of lesions and potential risk factors. Prev. Vet. Med., 108: 218-224. https://doi.org/10.1016/j.prevetmed.2012.07.015
Arias-Álvarez M., García-García R.M., Torres-Rovira L., González- Bulnes A., Rebollar P.G., Lorenzo P.L. 2010. Influence of hormonal and nonhormonal estrus synchronization methods on follicular and oocyte quality in primiparous lactating does at early postpartum period. Theriogenology, 73: 26-35. https://doi.org/10.1016/j.theriogenology.2009.07.017
Bánszegi O., Altbäcker V., Bilkó Á. 2009. Intrauterine position influences anatomy and behavior in domestic rabbits. Physiol. Behav., 98: 258-262. https://doi.org/10.1016/j.physbeh.2009.05.016
Bánszegi O., Szenczi P., Dombay K., Bilkó Á., Altbäcker V. 2012. Anogenital distance as a predictor of attractiveness, litter size and sex ratio of rabbit does. Physiol. Behav., 105: 1226-1230. https://doi.org/10.1016/j.physbeh.2012.01.002
Beehner J.C., Phillips-Conroy J.E., Whitten P.L. 2005. Female testosterone, dominance rank, and aggression in an Ethiopian population of hybrid baboons. Am. J. Primatol., 67, 101-119. https://doi.org/10.1002/ajp.20172
Bill J., Rauterberg S., Herbrandt S., Ligges U., Kemper N., Fels M., Agonistic behavior and social hierarchy in female domestic rabbits kept in semi-groups. J. Vet. Behav., 38: 21-31. https://doi.org/10.1016/j.jveb.2020.03.004
Braconnier M., Gómez Y., Gebhardt-Henrich S.G. 2020. Different regrouping schedules in semi group-housed rabbit does: Effects on agonistic behaviour, stress and lesions. Appl. Anim. Behav. Sci., 228: 105024. https://doi.org/10.1016/j.applanim.2020.105024
Buijs S., Maertens L., Hermans K., Vangeyte J., André F., Tuyttens M. 2015. Behaviour, wounds, weight loss and adrenal weight of rabbit does as affected by semigroup housing. Appl. Anim. Behav. Sci., 172: 44-51. https://doi.org/10.1016/j.applanim.2015.09.003
Buijs S., Vangeyte J., Tuyttens F.A.M. 2016. Effects of communal rearing and group size on breeding rabbits’ post-grouping behaviour and its relation to anogenital distance. Appl. Anim. Behav. Sci., 182: 53-60. https://doi.org/10.1016/j.applanim.2016.06.005
Carnaby K., Painer J., Söderberg A., Gavier-Widèn D., Göritz F., Dehnhard M., Jewgenow K. 2012. Histological and endocrine characterization of the annual luteal activity in Eurasian Lynx (Lynx lynx). Reproduction, 10.1530 / REP-12-0166 144: 477-483. https://doi.org/10.1530/REP-12-0166
Chu L.R., Garner J.P., Mench J.A., 2004. A behavioral comparison of New Zealand White rabbits (Oryctolagus cuniculus) housed individually or in pairs in conventional laboratory cages. Appl. Anim. Behav. Sci., 85: 121-139. https://doi.org/10.1016/j.applanim.2003.09.011
Dal Bosco A., Mugnai C., Martino M., Szendrő Z., Mattioli S., Cambiotti V., Cartoni Mancinelli A., Moscati L., Castellini C. 2019. Housing Rabbit Does in a Combi System with Removable Walls: Effect on Behaviour and Reproductive Performance. Animals, 9: 528-528. https://doi.org/10.3390/ani9080528
Davis E.S., Marler C.A. 2003. The progesterone challenge: steroid hormone changes following a simulated territorial intrusion in female Peromyscus californicus. Horm. Behav., Special Issue on Aggressive and Violent Behavior, 44: 185-198. https://doi.org/10.1016/S0018-506X(03)00128-4
Dehnhard M., Naidenko S., Frank A., Braun B., Göritz F., Jewgenow K. 2008. Non-invasive Monitoring of Hormones: A Tool to Improve Reproduction in Captive Breeding of the Eurasian Lynx. Reprod. Domest. Anim., 43: 74-82. https://doi.org/10.1111/j.1439-0531.2008.01145.x
Denenberg V.H., Sawin P.B., Frommer G.P., Ross S. 1958. Genetic, physiological and behavioral background of reproduction in the rabbit: IV. An analysis of maternal behavior at successive parturitions. Behaviour 13: 131-142. https://doi.org/10.1163/156853958X00073
Drickamer L.C. 1996. Intra-uterine position and anogenital distance in house mice: consequences under field conditions. Anim. Behav., 51: 925-934. https://doi.org/10.1006/anbe.1996.0096
Dušek A., Bartoš L. 2012. Variation in Ano-Genital Distance in Spontaneously Cycling Female Mice. Reprod. Domest. Anim., 47: 984-987. https://doi.org/10.1111/j.1439-0531.2012.02003.x
Fortun L., Prunier A., Lebas F. 1993. Effects of lactation on fetal survival and development in rabbit does mated shortly after parturition. J. Anim. Sci., 71: 1882-1886. https://doi.org/10.2527/1993.7171882x
Gobikrushanth M., Bruinjé T.C., Colazo M.G., Butler S.T., Ambrose D.J. 2017. Characterization of anogenital distance and its relationship to fertility in lactating Holstein cows. J. Dairy Sci., 100: 9815-9823. https://doi.org/10.3168/jds.2017-13033
González-Mariscal G., Díaz-Sánchez V., Melo A.I., Beyer C., Rosenblatt J.S. 1994. Maternal behavior in New Zealand white rabbits: Quantification of somatic events, motor patterns, and steroid plasma levels. Physiol. Behav., 55: 1081-1089. https://doi.org/10.1016/0031-9384(94)90391-3
González-Mariscal G., Jiménez P., Beyer C., Rosenblatt J.S. 2003. Androgens stimulate specific aspects of maternal nestbuilding and reduce food intake in rabbits. Horm. Behav., 43: 312-317. https://doi.org/10.1016/S0018-506X(02)00046-6
González-Mariscal G., Gallegos J.A., Sierra-Ramirez A., Flores J.G. 2009. Impact of concurrent pregnancy and lactation on maternal nest- building, estradiol and progesterone concentrations in rabbits. World Rabbit Sci., 17: 145-152. https://doi.org/10.4995/wrs.2009.654
González-Mariscal G., Lemus A.C., Vega-González A., Aguilar-Roblero A. 2013a. Litter size determines circadian periodicity of nursing in rabbits. Chronobiol. Int., 30: 711-718. https://doi.org/10.3109/07420528.2013.784769
González-Mariscal G., Toribio A., Gallegos-Huicochea J.A., Serrano-Meneses M.A. 2013b. The characteristics of suckling stimulation determine the daily duration of motheryoung contact and milk output in rabbits. Dev. Psychobiol. 55: 809-817. https://doi.org/10.1002/dev.21071
González-Mariscal G., Gallegos J.A. 2014. The maintenance and termination of maternal behavior in rabbits: Involvement of suckling and progesterone. Physiol. Behav., 124: 72-76. https://doi.org/10.1016/j.physbeh.2013.10.031
González-Mariscal G., Caba M., Martínez-Gómez M., Bautista A., Hudson R. 2016. Mothers and offspring: The rabbit as a model system in the study of mammalian maternal behavior and sibling interactions. Horm. Behav., 77: 30-41. https://doi.org/10.1016/j.yhbeh.2015.05.011
González-Mariscal G., Sisto Burt A., Nowak R. 2017. Behavioral and neuroendocrine indicators of well-being in farm and laboratory mammals. Pfaff D. & Joëlls M., eds. “Hormones, Brain and Behavior” 3a ed. Elsevier, 454-485. https://doi.org/10.1016/B978-0-12-803592-4.00017-1
Graf S., Bigler L., Failing K., Würbel H., Buchwalder T. 2011. Regrouping rabbit does in a familiar or novel pen: Effects on agonistic behaviour, injuries and core body temperature. Appl. Anim. Behav. Sci., 135: 121-127. https://doi.org/10.1016/j.applanim.2011.10.009
Hein D.J. 2019. Labordiagnostik bei Kleinsäugern: Präanalytik und tierartspezifische Befundung. Schlütersche. Hein J. 2014. Blutentnahme und Venenverweilkatheter beim Kaninchen. kleintier konkret 17: 23-25. https://doi.org/10.1055/s-0034-1384446
Hoffman K.L., Martínez-Alvarez E., Rueda-Morales R.I. 2009. The inhibition of female rabbit sexual behavior by progesterone: Progesterone receptor-dependent and-independent effects. Horm. Behav., 55: 84-92. https://doi.org/10.1016/j.yhbeh.2008.08.011
Holst D. von, Hutzelmeyer H., Kaetzke P., Khaschei M., Rödel H.G. 2002. Social rank, fecundity and lifetime reproductive success in wild European rabbits (Oryctolagus cuniculus). Behav. Ecol. Sociobiol., 51, 245–254. https://doi.org/10.1007/s00265-001-0427-1
Hudson R., Shaal B., Bilkó Á., Altbäcker V. 1996. Just three minutes a day: The behaviour of young rabbits viewed in the context of limited maternal care. In Proc.: 6th World Rabbit Congress, July 1996, Toulouse, France, 2: 395-403.
Hudson R., Shaal B., Martínez-Gómez M., Distel H. 2000. Mother–young relations in the European rabbit: physiological and behavioural locks and keys. World Rabbit Science 8: 85-90. https://doi.org/10.4995/wrs.2000.424
Kosowska B., Strzała T., Moska M., Ratajszczak R., Dobosz T. 2015. Cytogenetic Examination of South American Tapirs, Tapirus Terrestris (Perissodactyla, Tapiridae), from the Wroclaw Zoological Garden. Vestnik Zoologii, 49: 529-536.
Lebas F., Coudert P.,. de Rochambeau H.,. Thebault R.G. 1997. The rabbit - Husbandry, health and production. FAO Animal Production and Health Series No. 21.
Maertens L., Rommers J., Jacquet M. 2011. Le logement des lapins en parcs, une alternative pour les cages classiques dans un système “duo”? [Combi-park housing of females, an alternative for the classical cages when using the “duo” management system?]. 14èmes Journées de la Recherche Cunicole, 85-88.
Mann M.A., Svare B. 1982. Factors influencing pregnancy induced aggression in mice. Behav. Neural Biol., 36: 242-258. https://doi.org/10.1016/S0163-1047(82)90867-6
Mann M.A., Konen C., Svare B. 1984. The role of progesterone in pregnancy-induced aggression in mice. Horm. Behav., 18: 140-160. https://doi.org/10.1016/0018-506X(84)90039-4
Markvardsen S.N., Kjelgaard-Hansen M., Ritz C., SØrensen D.B. 2012. Less invasive blood sampling in the animal laboratory: Clinical chemistry and haematology of blood obtained by the triatominae bug Dipetalogaster maximus. Lab. Anim., 46: 136-141. https://doi.org/10.1258/la.2011.011063
Mira-Escolano M.P., Mendiola J., Mínguez-Alarcón L., Melgarejo M., Cutillas-Tolín A., Roca M., López-Espín J.J., Noguera-Velasco J.A., Torres-Cantero A.M. 2014. Longer anogenital distance is associated with higher testosterone levels in women: a cross-sectional study. BJOG, 121: 1359-1364. https://doi.org/10.1111/1471-0528.12627
Mugnai C., Dal Bosco A., Castellini C. 2009. Effect of different rearing systems and pre-kindling handling on behaviour and performance of rabbit does. Appl. Anim. Behav. Sci., 118: 91-100. https://doi.org/10.1016/j.applanim.2009.02.007
Nielsen S.S., Alvarez J., Bicout D.J., Calistri P., Depner K., Drewe J.A., Garin-bastuji B., Luis J., Rojas G., Michel V., Angel M., Chueca M., Roberts H.C., Sihvonen L.H., Spoolder H., Stahl K., Calvo A.V., Viltrop A., Buijs S., Edwards S., Candiani D., Mosbach-schulz O. 2020. Health and welfare of rabbits farmed in different production systems, EFSA J., 18: 1-96. https://doi.org/10.2903/j.efsa.2020.5944
O’Malley B. 2005. Rabbits. In: O’Malley B. (Ed.), Clinical Anatomy and Physiology of Exotic Species. Elsevier, New York, pp. 173-195. https://doi.org/10.1016/B978-070202782-6.50011-9
Palanza P., Parmigiani S., Vom Saal F.S. 1995. Urine marking and maternal aggression of wild female mice in relation to anogenital distance at birth. Physiol. Behav., 58: 827-835. https://doi.org/10.1016/0031-9384(95)00107-T
Palka Y.S., Sawyer C.H. 1966. The effects of hypothalamic implants of ovarian steroids on oestrous behaviour in rabbits. J. Physiol., 185: 251-269. https://doi.org/10.1113/jphysiol.1966.sp007986
R Core Team, 2019., A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rödel H.G., Monclús R., von Holst D. 2006. Behavioral styles in European rabbits: Social interactions and responses to experimental stressors. Physiol. Behav., 89: 180-188. https://doi.org/10.1016/j.physbeh.2006.05.042
Rödel H.G., Starkloff A., Bautista A., Friedrich A.C., Von Holst D. 2008. Infanticide and maternal offspring defence in European rabbits under natural breeding conditions. Ethology, 114: 22-31. https://doi.org/10.1111/j.1439-0310.2007.01447.x
Rommers J.M., Gunnink H., Klop A., De Jong I.C. 2011. Dynamics in aggressive behaviour of rabbit does in a group housing system: a descriptive study. In: 17th International Symposium on Housing and Diseases of Rabbits, Fur Providing Animals and Pet Animals, May 11-12. Celle, Germany, pp. 75-85.
Rommers J.M., Reuvekamp B.J.F., Gunnink H., de Jong I.C. 2014. Effect of hiding places, straw and territory on aggression in group-housed rabbit does. Appl. Anim. Behav. Sci., 157: 117-126. https://doi.org/10.1016/j.applanim.2014.05.011
Schönbrodt F.D., Perugini M. 2013. At what sample size do correlations stabilize? J. Res. Pers., 47: 609-612. https://doi.org/10.1016/j.jrp.2013.05.009
Shargal D., Shore L., Roteri N., Terkel A., Zorovsky Y., Shemesh M., Steinberger Y. 2008. Fecal testosterone is elevated in high ranking female ibexes (Capra nubiana) and associated with increased aggression and a preponderance of male offspring. Theriogenology 69: 673-680. https://doi.org/10.1016/j.theriogenology.2007.11.017
Simpson E.R. 2002. Aromatization of androgens in women: current concepts and findings. Fertil. Steril., 77: 6-10. https://doi.org/10.1016/S0015-0282(02)02984-9
Squire L.R. 2009. Encyclopedia of Neuroscience, Volume 1. Academic Press. https://doi.org/10.1093/acprof:oso/9780195380101.003.0001
Stadler A., Meiser C.K., Schaub G. a. 2011. “Living Syringes”: use of Haematophagous Bugs as Blood Samplers from Small and Wild Animals. Nature Helps... 243-272. https://doi.org/10.1007/978-3-642-19382-8
Szendrő Z., McNitt J.I., Matics Z., Mikó A., Gerencsér Z. 2016. Alternative and enriched housing systems for breeding does: A review. World Rabbit Sci., 24: 1-14. https://doi.org/10.4995/wrs.2016.3801
Takahashi, Kayo, Hosoya T., Onoe K., Takashima T., Tanaka M., Ishii A., Nakatomi Y., Tazawa S., Takahashi, Kazuhiro, Doi H., Wada Y., Watanabe Y. 2018. Association between aromatase in human brains and personality traits. Sci. Rep., 8: 1-9. https://doi.org/10.1038/s41598-018-35065-4
Theau-Clément M., Poujardien B., Bellereaud J. 1990. Influence des traitements lumineux, modes de reproduction et états physiologiques sur la productivité de lapines multipares. In: 5èmes Journées de La Recherche Cunicole, Dec 1990, Paris, France.
Thomsen R., Voigt C.C. 2006. Non-invasive blood sampling from primates using laboratory-bred blood-sucking bugs (Dipetalogaster maximus; Reduviidae, Heteroptera). Primates, 47: 397-400. https://doi.org/10.1007/s10329-006-0194-8
Trainor B.C., Bird I.M., Marler C.A. 2004. Opposing hormonal mechanisms of aggression revealed through short-lived testosterone manipulations and multiple winning experiences. Horm. Behav., 45: 115-121. https://doi.org/10.1016/j.yhbeh.2003.09.006
Trainor B.C., Kyomen H.H., Marler C.A. 2006. Estrogenic encounters: How interactions between aromatase and the environment modulate aggression. Front. Neuroendocrinol., 27: 170-179. https://doi.org/10.1016/j.yfrne.2005.11.001
Ubilla E., Rebollar P.G. 1995. Influence of the postpartum day on plasma estradiol-17 β levels, sexual behaviour, and conception rate, in artificially inseminated lactating rabbits. Anim. Reprod. Sci., 38: 337-344. https://doi.org/10.1016/0378-4320(94)01366-T
Voigt C.C., Von Helversen O., Michener R.H., Kunz T.H. 2003. Validation of a Non-Invasive Blood-Sampling Technique for Doubly-Labelled Water Experiments. J. Exp. Zool. A Comp. Exp. Biol., 296: 87-97. https://doi.org/10.1002/jez.a.10121
Voigt C.C., Faßbender M., Dehnhard M., Wibbelt G., Jewgenow K., Hofer H., Schaub G.A. 2004. Validation of a minimally invasive blood-sampling technique for the analysis of hormones in domestic rabbits, Oryctolagus cuniculus (Lagomorpha). Gen. Comp. Endocrinol., 135: 100-107. https://doi.org/10.1016/j.ygcen.2003.08.005
Voigt C.C., Peschel U., Wibbelt G., Frölich K. 2006. An Alternative, Less Invasive Blood Sample Collection Technique for Serologic Studies Utilizing Triatomine Bugs (Heteroptera; Insecta). J. Wildl. Dis., 42: 466-469. https://doi.org/10.7589/0090-3558-42.2.466
von Engelhard N., Kappeler P.M., Heistermann M. 2000. Androgen levels and female social dominance in Lemur catta. In Proc.: R. Soc. Lond. B, 267: 1533-1539. https://doi.org/10.1098/rspb.2000.1175
Vos A.C., Müller T., Neubert L., Voigt C.C. 2010. Validation of a Less Invasive Blood Sampling Technique in Rabies Serology Using Reduviid Bugs (Triatominae, Hemiptera). J. Zoo. Wildl. Med., 41: 63-68. https://doi.org/10.1638/2009-0103.1
Wingfield J.C., Hegner R.E., Dufty, Alfred M., Ball G.F. 1990. The “Challenge Hypothesis”: Theoretical Implications for Patterns of Testosterone Secretion, Mating Systems, and Breeding Strategies. Am. Nat., 136: 829-846. https://doi.org/10.1086/285134
Zomeño C., Birolo M., Zu A., Xiccato G., Trocino A. 2017. Aggressiveness in group-housed rabbit does: Influence of group size and pen characteristics. Appl. Anim. Behav. Sci., 194: 79-85. https://doi.org/10.1016/j.applanim.2017.05.016
Zomeño C., Birolo M., Gratta F., Zuffellato A., Xiccato G., Trocino A. 2018. Effects of group housing system, pen floor type, and lactation management on performance and behaviour in rabbit does. Appl. Anim. Behav. Sci., 203: 55-63. https://doi.org/10.1016/j.applanim.2018.03.002
Downloads
Published
Issue
Section
License
This journal is licensed under a "Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)".