Timing of maternal nest building and perinatal offspring survival in a group-living small mammal

  • Martin W. Seltmann
  • Marylin Rangassamy
  • Manuela Zapka
  • Kurt L. Hoffman
  • Heiko G. Rödel
Original Article


Maternal care frequently includes the construction of a burrow or nest where mothers will raise their young. Delays in the timing of such complex sequences of building behavior might potentially interfere with mothers’ successful reproduction. By analyzing a long-term data set (11 years) from a study on European rabbits Oryctolagus cuniculus, we tested whether late maternal burrow and nest building increases the occurrence of perinatal offspring mortality. Additionally, we aimed to identify causes for the occurrence of such late burrow and nest building behavior. In the majority of cases, mothers dug their nursery burrow and constructed a grass nest inside well before the last 24 h prior to parturition. During the last pre-partum day, mothers usually lined the nests with their abdominal hair. However, when mothers carried out of all these activities during the last 24 h pre-partum (“late burrow and nest building”), perinatal mortality was significantly increased. Social constraints might have affected the temporal aspects of females’ display of nest building. Thus, in social groups occupying smaller territories, late burrow and nest building occurred with a significantly higher probability when several females of that group gave birth within a period of a few days (“concurrent parturition”). Behavioral observations suggested that concurrent parturition was associated a higher level of intra-sexual competition, since a significantly increased frequency of agonistic interactions among females was observed in these conditions. The results suggest a mechanism by which the mothers’ social environment influences perinatal mortality, thus adding to our knowledge on drivers of maternal fitness.

Significance statement

Differences in the timing of maternal care behavior can strongly affect offspring survival. We investigated this link in a long-term study of a colony of European rabbits. In this species, the young are born and raised in nests situated in nursery burrows dug by the mother. Females which dug their burrow and constructed the nest during the last night before giving birth showed a higher perinatal offspring mortality than mothers that dug their burrow earlier. Furthermore, we explored potential causes of such delays in the timing of burrow and nest construction. Agonistic social interactions between females were increased when different females of a group reproduced at around the same time. Overall, the findings support the conclusion that competition for breeding resources, in particular within smaller group territories, was an important driver for delays in maternal burrow and nest building.


Early survival European rabbit Female competition Maternal effects Social behavior 



We are grateful to Dietrich von Holst for his kind support and for helpful comments on the manuscript. We are also grateful to the two reviewers of this manuscript for their constructive comments and suggestions. We thank all students who helped with the field work during the years of study, and we thank Margaux Babola who assisted to extract the data sets from the long-term database.

Compliance with ethical standards


This research was partly supported by a grant to HGR from the German Research Foundation DFG (RO 2431/2-1, 2). MWS was funded by the Finnish Society for Sciences and Letters, by the Societas pro Fauna et Flora Fennica, and by a travel grant provided by the Institut Francilien d’Ethologie IFE and by the Université Paris 13.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed. Permission for the studies on European rabbits was granted by the government of Middle Franconia, Germany (211-3894a), and was approved by the institutional animal welfare officer.

Supplementary material

265_2017_2296_MOESM1_ESM.docx (42 kb)
ESM 1 (DOCX 41.8 kb)


  1. Adams N, Boice R (1981) Mouse (Mus) burrows: effects of age, strain, and domestication. Anim Learn Behav 9:140–144CrossRefGoogle Scholar
  2. Albrecht ED, Nightingale MS, Towsley JD (1977) Stress-induced decreases in the serum concentration of progesterone in the pregnant baboon. J Endocrinol 77:425–426CrossRefGoogle Scholar
  3. Aldomy F, Hussein NO, Sawalha L, Khatatbeh K, Aldomy A (2009) A national survey of perinatal mortality in sheep and goats in Jordan. Pak Vet J 29:102–106Google Scholar
  4. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  5. Bautista A, Drummond H, Martínez-Gómez M, Hudson R (2003) Thermal benefit of sibling presence in the newborn rabbit. Dev Psychobiol 43:208–215CrossRefPubMedGoogle Scholar
  6. Blanchard DC, Spencer RL, Weiss SM, Blanchard RJ, McEwen BS, Sakai RR (1995) Visible burrow system as a model of chronic social stress: behavioural and neuroendocrine correlates. Psychoneuroendocrinology 20:117–134CrossRefPubMedGoogle Scholar
  7. Bouchard PR, Lynch CB (1989) Burrowing behavior in wild house mice: variation within and between populations. Behav Genet 19:447–456CrossRefPubMedGoogle Scholar
  8. Brambell FWR (1944) The reproduction of the wild rabbit, Oryctolagus cuniculus (L.) Proc Zool Soc Lond 114:1–45CrossRefGoogle Scholar
  9. Broekhuizen S, Mulder JL (1983) Differences and similarities in nursing behaviour of hares and rabbits. Acta Zool Fenn 174:61–63Google Scholar
  10. Bult A, Lynch CB (1996) Multiple selection responses in house mice bidirectionally selected for thermoregulatory nest-building behavior: crosses of replicate lines. Behav Genet 26:439–446CrossRefPubMedGoogle Scholar
  11. Bult A, Lynch CB (1997) Nesting and fitness: lifetime reproductive success in house mice bidirectionally selected for thermoregulatory nest-building behavior. Behav Genet 27:231–240CrossRefPubMedGoogle Scholar
  12. Canali E, Ferrante V, Todeschini R, Verga M, Carenzi C (1991) Rabbit nest construction and its relationship with litter development. Appl Anim Behav Sci 31:259–266CrossRefGoogle Scholar
  13. Christian JJ (1980) Endocrine factors in population regulation. In: Cohen MN, Malpass RS, Klein HG (eds) Biosocial mechanisms of population regulation. Yale University Press, Yale, pp 55–115Google Scholar
  14. Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, PrincetonGoogle Scholar
  15. Collias EC, Collias NE (1964) The development of nest building in a weaverbird. Auk 81:42–52CrossRefGoogle Scholar
  16. Coureaud G, Rödel HG, Le Normand B, Fortun-Lamothe L, Bignon L (2015) Habitat et comportement. In: Gidenne T (ed) Le lapin: De la biologie à l’élevage. Éditions Quæ, Versailles, pp 107–136Google Scholar
  17. Cowan DP (1987) Aspects of the social organization of the European wild rabbit (Oryctolagus cuniculus). Ethology 75:197–210CrossRefGoogle Scholar
  18. Creeth H, McNamara G, Tunster S, Eddy J, Isles A, John R (2015) Programming of maternal behaviour by the placenta: a novel animal model. Psychoneuroendocrinology 61:4 (abstract) CrossRefPubMedGoogle Scholar
  19. Denenberg VH, Sawin PB, Frommer GP, Ross S (1958) Genetic, physiological and behavioral background of reproduction in the rabbit: IV. An analysis of maternal behavior at successive parturitions. Behaviour 13:131–142CrossRefGoogle Scholar
  20. Denenberg VH, Petropolus SF, Sawin PB, Ross S (1960) Genetic, physiological and behavioral background of reproduction in the rabbit: VI. Maternal behavior with reference to scattered and cannibalized newborn and mortality. Behaviour 15:71–76CrossRefGoogle Scholar
  21. Denenberg VH, Huff RL, Ross S, Sawin PB, Zarrow MX (1963) Maternal behaviour in the rabbit: the quantification of nest building. Anim Behav 11:494–499CrossRefGoogle Scholar
  22. Dennis SM (1974) Perinatal lamb mortality in Western Australia. 1. General procedures and results. Aust Vet J 50:443–449CrossRefPubMedGoogle Scholar
  23. Deutsch JA (1957) Nest building behaviour of domestic rabbits under semi-natural conditions. Brit J Anim Behav 5:53–54CrossRefGoogle Scholar
  24. Farghaly HM (1996) Genetic and maternal variance components of stillbirths and pre-weaning mortality in purebred rabbits. Indian J Anim Sci 66:907–913Google Scholar
  25. Festa-Bianchet M (1988) Nursing behaviour of bighorn sheep: correlates of ewe age, parasitism, lamb age, birthdate and sex. Anim Behav 36:1445–1454CrossRefGoogle Scholar
  26. Forslund P, Pärt T (1995) Age and reproduction in birds—hypotheses and tests. Trends Ecol Evol 10:374–378CrossRefPubMedGoogle Scholar
  27. Fuchs AR, Dawood Y (1980) Oxytocin release and uterine activation during parturition in rabbits. Endocrinology 107:1117–1126CrossRefPubMedGoogle Scholar
  28. Gilbert C, Blanc S, Giroud S, Trabalon M, Le Maho Y, Perret M, Ancel A (2007) Role of huddling on the energetic of growth in a newborn altricial mammal. Am J Physiol-Reg I 293:R867–R876Google Scholar
  29. Giraudoux P (2016) pgirmess: data analysis in ecology. R package version 1.6.4.,
  30. González-Mariscal G, Rosenblatt JS (1996) Maternal behavior in rabbits: a historical and multidisciplinary perspective. Adv Stud Behav 25:333–360CrossRefGoogle Scholar
  31. González-Mariscal G, Díaz-Sánchez V, Melo AI, Beyer C, Rosenblatt JS (1994) Maternal behavior in New Zealand white rabbits: quantification of somatic events, motor patterns, and steroid plasma levels. Physiol Behav 55:1081–1089CrossRefPubMedGoogle Scholar
  32. González-Mariscal G, Melo AI, Jimenez P, Beyer C, Rosenblatt JS (1996) Estradiol, progesterone, and prolactin regulate maternal nest-building in rabbits. J Neuroendocrinol 8:901–907CrossRefPubMedGoogle Scholar
  33. González-Mariscal G, Gallegos JA, Sierra-Ramírez A, Garza Flores J (2009) Impact of concurrent pregnancy and lactation on maternal nestbuilding, estradiol and progesterone concentrations in rabbits. World Rabbit Sci 17:145–152Google Scholar
  34. González-Mariscal G, Lemus AC, Vega-Gonzalez A, Aguilar-Roblero R (2013) Litter size determines circadian periodicity of nursing in rabbits. Chronobiol Int 30:711–718CrossRefPubMedGoogle Scholar
  35. 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 77:30–41CrossRefPubMedGoogle Scholar
  36. González-Redondo P (2010) Maternal behaviour in peripartum influences preweaning kit mortality in cage-bred wild rabbits. World Rabbit Sci 18:91–102CrossRefGoogle Scholar
  37. Gundlach H (1968) Brutfürsorge, Brutpflege, Verhaltensontogenese und Tagesperiodik beim Europäischen Wildschwein (Sus scrofa L.) Z Tierpsychol 25:955–995PubMedGoogle Scholar
  38. Hall ZJ, Meddle SL, Healy SD (2015) From neurons to nests: nest-building behaviour as a model in behavioural and comparative neuroscience. J Ornithol 156:133–143CrossRefPubMedPubMedCentralGoogle Scholar
  39. Hansell M (2000) Bird nests and construction behaviour. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  40. Hansell M (2005) Animal architecture. Oxford University Press, OxfordCrossRefGoogle Scholar
  41. Hoffman KL, González-Mariscal G (2006) Progesterone receptor activation signals behavioral transitions across the reproductive cycle of the female rabbit. Horm Behav 50:154–168CrossRefPubMedGoogle Scholar
  42. Hoffman KL, Martínez-Alvarez E, Rueda-Morales RI (2009) The inhibition of female rabbit sexual behavior by progesterone: progesterone receptor-dependent and-independent effects. Horm Behav 55:84–92CrossRefPubMedGoogle Scholar
  43. Holm S (1979) A simple sequential rejective multiple test procedure. Scand J Stat 6:65–70Google Scholar
  44. Hudson R, Bilkó Á, Altbäcker V (1996) Nursing, weaning and the development of independent feeding in the rabbit (Oryctolagus cuniculus). Z Säugetierkd 61:39–48Google Scholar
  45. Hudson R, Cruz Y, Lucio RA, Nimomiya J, Martínez-Gómez M (1999) Temporal and behavioral patterning of parturition in rabbits and rats. Physiol Behav 66:599–604CrossRefPubMedGoogle Scholar
  46. Hull D (1973) Thermoregulation in young mammals. In: Whittow GC (ed) Comparative physiology of thermoregulation: special aspects of thermoregulation. Academic, New York, pp 167–200CrossRefGoogle Scholar
  47. Jilge B (1993) The ontogeny of circadian rhythms in the rabbit. J Biol Rhythm 8:247–260CrossRefGoogle Scholar
  48. Kalin NH, Gibbs DM, Barksdale CM, Shelton SE, Carnes M (1985) Behavioral stress decreases plasma oxytocin concentrations in primates. Life Sci 36:1275–1280CrossRefPubMedGoogle Scholar
  49. Kendeigh SC (1952) Parental care and its evolution in birds. University of Illinois Press, UrbanaCrossRefGoogle Scholar
  50. Klein SL, Nelson RJ (1999) Influence of social factors on immune function and reproduction. Rev Reprod 4:168–178CrossRefPubMedGoogle Scholar
  51. Koivula M, Koskela E, Mappes T, Oksanen TA (2003) Cost of reproduction in the wild: manipulation of reproductive effort in the bank vole. Ecology 84:398–405CrossRefGoogle Scholar
  52. Leng G, Mansfield S, Bicknell RJ, Brown D, Chapman C, Hollingsworth S, Ingram CD, Marsh MI, Yates JO, Dyer RG (1987) Stress-induced disruption of parturition in the rat may be mediated by endogenous opioids. J Endocrinol 114:247–252CrossRefPubMedGoogle Scholar
  53. Lessells CM, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk 104:116–121CrossRefGoogle Scholar
  54. Lombardo MP (1994) Nest architecture and reproductive performance in tree swallows (Tachycineta bicolor). Auk 111:814–824CrossRefGoogle Scholar
  55. Mainwaring MC, Hartley IR (2013) The energetic costs of nest building in birds. Avian Biol Res 6:12–17CrossRefGoogle Scholar
  56. Martin P, Bateson P (1986) Measuring behaviour: an introductory guide. Cambridge University Press, CambridgeGoogle Scholar
  57. Mellor DJ, Stafford KJ (2004) Animal welfare implications of neonatal mortality and morbidity in farm animals. Vet J 168:118–133CrossRefPubMedGoogle Scholar
  58. Mila H, Grellet A, Feugier A, Chastant-Maillard S (2015) Differential impact of birth weight and early growth on neonatal mortality in puppies. J Anim Sci 93:4436–4442CrossRefPubMedGoogle Scholar
  59. Millar JS (2007) Nest mortality in small mammals. Ecoscience 14:286–291CrossRefGoogle Scholar
  60. Murgatroyd CA, Nephew BC (2013) Effects of early life social stress on maternal behavior and neuroendocrinology. Psychoneuroendocrinology 38:219–228CrossRefPubMedGoogle Scholar
  61. Myers K, Poole WE (1961) A study of the biology of the wild rabbit, Oryctolagus cuniculus (L.), in confined populations. II. The effects of season and population increase on behaviour. Wildlife Res 6:1–41CrossRefGoogle Scholar
  62. Mykytowycz R (1958) Social behaviour of an experimental colony of wild rabbits (Oryctolagus cuniculus L.) I. Establishment of the colony. Wildlife Res 3:7–25CrossRefGoogle Scholar
  63. Mykytowycz R, Fullagar PJ (1973) Effects of social environment on reproduction in the rabbit, Oryctolagus cuniculus (L.) J Reprod Fertil 19:503–522Google Scholar
  64. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956PubMedGoogle Scholar
  65. Pittet F, Coignard M, Houdelier C, Richard-Yris MA, Lumineau S (2012) Age affects the expression of maternal care and subsequent behavioural development of offspring in a precocial bird. PLoS One 7:e36835CrossRefPubMedPubMedCentralGoogle Scholar
  66. R Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna Google Scholar
  67. Rachlow JL, Sanchez DM, Estes-Zumpf WA (2005) Natal burrows and nests of free-ranging pygmy rabbits (Brachylagus idahoensis). Monogr West N Am Nat 65:136–139Google Scholar
  68. Rödel HG, Bora A, Kaiser J, Kaetzke P, Khaschei M, von Holst D (2004) Density-dependent reproduction in the European rabbit: a consequence of individual response and age-dependent reproductive performance. Oikos 104:529–539CrossRefGoogle Scholar
  69. Rödel HG, Starkloff A, Bautista A, Friedrich AC, von Holst D (2008a) Infanticide and maternal offspring defence in European rabbits under natural breeding conditions. Ethology 114:22–31CrossRefGoogle Scholar
  70. Rödel HG, Starkloff A, Bruchner B, von Holst D (2008b) Social environment and reproduction in female European rabbits (Oryctolagus cuniculus): benefits of the presence of litter sisters. J Comp Psychol 122:73–83CrossRefPubMedGoogle Scholar
  71. Rödel HG, Prager G, Stefanski V, von Holst D, Hudson R (2008c) Separating maternal and litter size effects on early postnatal growth in two species of altricial mammals. Physiol Behav 93:826–834CrossRefPubMedGoogle Scholar
  72. Rödel HG, Starkloff A, Seltmann MW, Prager G, von Holst D (2009a) Causes and predictors of nest mortality in a European rabbit population. Mamm Biol 74:198–209CrossRefGoogle Scholar
  73. Rödel HG, von Holst D, Kraus C (2009b) Family legacies: short- and long-term fitness consequences of early-life conditions in female European rabbits. J Anim Ecol 78:789–797CrossRefPubMedGoogle Scholar
  74. Rödel HG, Dausmann KH, Starkloff A, Schubert M, von Holst D, Hudson R (2012) Diurnal nursing pattern of wild-type European rabbits under natural breeding conditions. Mamm Biol 77:441–446CrossRefGoogle Scholar
  75. Rodríguez-Martínez L, Hudson R, Martínez-Gómez M, Bautista A (2013) Description of the nursery burrow of the Mexican cottontail rabbit Sylvilagus cunicularius under seminatural conditions. Acta Theriol 59:193–201CrossRefGoogle Scholar
  76. Ross S, Denenberg VH, Sawin PB, Meyer P (1956) Genetic, physiological and behavioral background of reproduction in the rabbit: IV. An analysis of maternal behavior at successive parturitions. Brit J Anim Behav 4:69–70CrossRefGoogle Scholar
  77. Ross S, Zarrow MX, Sawin PB, Denenberg VH, Blumenfield M (1963) Maternal behaviour in the rabbit under semi-natural conditions. Anim Behav 11:283–285CrossRefGoogle Scholar
  78. Royle NJ, Smiseth PT, Kölliker M (2012) The evolution of parental care. Oxford University Press, OxfordCrossRefGoogle Scholar
  79. Sapolsky RM (1992) Neuroendocrinology of the stress-response. In: Becker JB, Breedlove SM, Crews D (eds) Behavioral endocrinology. MIT Press, Cambridge, pp 287–324Google Scholar
  80. Sapolsky RM (1993) Endocrinology alfresco: psychoendocrine studies of wild baboons. Recent Prog Horm Res 48:437–468CrossRefPubMedGoogle Scholar
  81. Stanton HC, Carroll JK (1974) Potential mechanisms responsible for prenatal and perinatal mortality or low viability of swine. J Anim Sci 38:1037–1044CrossRefPubMedGoogle Scholar
  82. Tandu-Umba B, Dedetemo DK, Mananga GL (2014) Maternal stress and pregnancy outcomes. Open J Obstet Gynecol 4:361–370CrossRefGoogle Scholar
  83. Torche F (2011) The effect of maternal stress on birth outcomes: exploiting a natural experiment. Demography 48:1473–1479CrossRefPubMedGoogle Scholar
  84. von Holst D (1998) The concept of stress and its relevance for animal behavior. Adv Stud Behav 27:1–131CrossRefGoogle Scholar
  85. von Holst D (2001) Social stress in wild mammals in their natural habitat. In: Broom DM (ed) Coping with challenge: welfare in animals including humans. Dahlem University Press, Berlin, pp 317–335Google Scholar
  86. von Holst D, Hutzelmeyer H, Kaetzke P, Khaschei M, Rödel HG, Schrutka H (2002) Social rank, fecundity and lifetime reproductive success in wild European rabbits (Oryctolagus cuniculus). Behav Ecol Sociobiol 51:245–254CrossRefGoogle Scholar
  87. Wang Z, Novak MA (1994) Parental care and litter development in primiparous and multiparous prairie voles (Microtus ochrogaster). J Mammal 75:18–23CrossRefGoogle Scholar
  88. Wiebold JL, Stanfield PH, Becker WC, Hiller JK (1986) The effect of restraint stress in early pregnancy mice. J Reprod Fertil 35:183–186Google Scholar
  89. Yamada F, Cervantes F (2005) Pentalagus furnessi. Mamm Spec 782:1–5CrossRefGoogle Scholar
  90. Ylönen H, Koskela E, Mappes T (1997) Infanticide in the bank vole (Clethrionomys glareolus): occurrence and the effect of familiarity on female infanticide. Ann Zool Fenn 34:259–266Google Scholar
  91. Zarrow MX, Denenberg VH, Kalberer WD (1965) Strain differences in the endocrine basis of maternal nest-building in the rabbit. J Reprod Fertil 10:397–401CrossRefPubMedGoogle Scholar
  92. Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Method Ecol Evol 1:3–14CrossRefGoogle Scholar
  93. Żurowski W (1992) Building activity of beavers. Acta Theriol 37:403–411CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Martin W. Seltmann
    • 1
    • 2
    • 3
    • 4
  • Marylin Rangassamy
    • 1
  • Manuela Zapka
    • 2
  • Kurt L. Hoffman
    • 5
  • Heiko G. Rödel
    • 1
    • 2
  1. 1.Laboratoire d’Ethologie Expérimentale et Comparée EA 4443Université Paris 13, Sorbonne Paris CitéVilletaneuseFrance
  2. 2.Animal PhysiologyUniversity of BayreuthBayreuthGermany
  3. 3.Faculty of Science and EngineeringÅbo Akademi UniversityTurkuFinland
  4. 4.Department of BiologyUniversity of TurkuTurkuFinland
  5. 5.Centro de Investigación en Reproducción Animal (CIRA)Universidad Autónoma de Tlaxcala CINVESTAVTlaxcalaMexico

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