SpringerLink
Log in

Parental Behavior in Rodents

  • Chapter
  • First Online:
Patterns of Parental Behavior

Part of the book series: Advances in Neurobiology ((NEUROBIOL,volume 27))

Abstract

Members of the order Rodentia are among the best-studied mammals for understanding the patterns, outcomes, and biological determinants of maternal and paternal caregiving. This research has provided a wealth of information but has historically focused on just a few rodents, mostly members of the two Myomorpha families that easily breed and can be studied within a laboratory setting (including laboratory rats, mice, hamsters, voles, gerbils). It is unclear how well this small collection of animals represents the over 2000 species of extant rodents. This chapter provides an overview of the hormonal and neurobiological systems involved in parental care in rodents, with a purposeful eye on providing information known or could be gleaned about parenting in various less-traditional members of Rodentia. We conclude from this analysis that the few commonly studied rodents are not necessarily even representative of the highly diverse members of Myomorpha, let alone other rodent suborders, and that additional laboratory and field studies of members of this order more broadly would surely provide invaluable information toward revealing a more representative picture of the rich diversity in rodent parenting.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
EUR 29.95
Price includes VAT (France)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
EUR 85.59
Price includes VAT (France)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
EUR 105.49
Price includes VAT (France)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info
Hardcover Book
EUR 105.49
Price includes VAT (France)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free ship** worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  • Adejumo DO, Adeyanju TA, Adeyanju TE. Range extension and first confirmed record of the Flightless Anomalure Zenkerella insignis (Matschie, 1898) (Mammalia: Rodentia: Anomaluridae) in Nigeria. J Threat Taxa. 2020;12(13):16900–3.

    Article  Google Scholar 

  • Ahdieh HB, Mayer AD, Rosenblatt JS. Effects of brain antiestrogen implants on maternal behavior and on postpartum estrus in pregnant rats. Neuroendocrinology. 1987;46(6):522–31.

    Article  CAS  PubMed  Google Scholar 

  • Akther S, Korshnova N, Zhong J, Liang M, Cherepanov SM, Lopatina O, Komleva YK, Salmina AB, Nishimura T, Fakhrul AA, Hirai H, Kato I, Yamamoto Y, Takasawa S, Okamoto H, Higashida H. CD38 in the nucleus accumbens and oxytocin are related to paternal behavior in mice. Mol Brain. 2013;6:41.

    Article  PubMed  PubMed Central  Google Scholar 

  • Albin-Brooks C, Nealer C, Sabihi S, Haim A, Leuner B. The influence of offspring, parity, and oxytocin on cognitive flexibility during the postpartum period. Horm Behav. 2017;89:130–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andersen DC. Observations on reproduction, growth, and behavior of the northern pocket gopher (Thomomys talpoides). J Mammal. 1978;59:418–22.

    Article  Google Scholar 

  • Antonini R, Turner TT, Pauerstein CJ. The hormonal control of the guinea pig corpus luteum during early pregnancy. Comp Study Fertil Steril. 1976;27(11):1322–5.

    Article  CAS  Google Scholar 

  • Asher M, Spinelli de Oliveira E, Sachser N. Social system and spatial organization of wild guinea pigs (Cavia aperea) in a natural population. J Mammal. 2004;85(4):788–96.

    Article  Google Scholar 

  • Aspillaga-Cid A, Vera DC, Ebensperger LA, Correa LA. Parental care in male degus (Octodon degus) is flexible and contingent upon female care. Physiol Behav. 2021;238:113487.

    Article  CAS  PubMed  Google Scholar 

  • Bakowska JC, Morrell JI. Atlas of the neurons that express mRNA for the long form of the prolactin receptor in the forebrain of the female rat. J Comp Neurol. 1997;386(2):161–77.

    Article  CAS  PubMed  Google Scholar 

  • Bale TL, Pedersen CA, Dorsa DM. CNS oxytocin receptor mRNA expression and regulation by gonadal steroids. Adv Exp Med Biol. 1995;395:269–80.

    CAS  PubMed  Google Scholar 

  • Bales KL, Saltzman W. Fathering in rodents: neurobiological substrates and consequences for offspring. Horm Behav. 2016;77:249–59.

    Article  CAS  PubMed  Google Scholar 

  • Bales KL, Kim AJ, Lewis-Reese AD, Sue Carter C. Both oxytocin and vasopressin may influence alloparental behavior in male prairie voles. Horm Behav. 2004;45:354–61.

    Article  CAS  PubMed  Google Scholar 

  • Bamshad M, Novak MA, De Vries GJ. Sex and species differences in the vasopressin innervation of sexually naive and parental prairie voles, Microtus ochrogaster and meadow voles, Microtus pennsylvanicus. J Neuroendocrinol. 1993;5:247–55.

    Article  CAS  PubMed  Google Scholar 

  • Bamshad M, Novak MA, de Vries GJ. Cohabitation alters vasopressin innervation and paternal behavior in prairie voles (Microtus ochrogaster). Physiol Behav. 1994;56:751–8.

    Article  CAS  PubMed  Google Scholar 

  • Barrière DA, Ella A, Szeremeta F, Adriaensen H, Même W, Chaillou E, Migaud M, Même S, Lévy F, Keller M. Brain orchestration of pregnancy and maternal behavior in mice. BioRxiv. 2020; https://doi.org/10.1101/2020.05.23.112045.

  • Barrington BA. Description of Birth and Young of the Pocket Gopher, Geomys Floridanus. J Mammal. 1942;23:428–30.

    Article  Google Scholar 

  • Baum MJ. Failure of pituitary transplants to facilitate the onset of maternal behavior in ovariectomized virgin rats. Physiol Behav. 1978;20(1):87–9.

    Article  CAS  PubMed  Google Scholar 

  • Bendesky A, Kwon Y-M, Lassance J-M, Lewarch CL, Yao S, Peterson BK, He MX, Dulac C, Hoekstra HE. The genetic basis of parental care evolution in monogamous mice. Nature. 2017;544:434–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Benedetto L, Rivas M, Pereira M, Ferreira A, Torterolo P. A descriptive analysis of sleep and wakefulness states during maternal behaviors in postpartum rats. Arch Ital Biol. 2017;155(3):99–109.

    CAS  PubMed  Google Scholar 

  • Bidau CJ, Patton JL, Pardiñas UFJ, D’Elía G. Mammals of South America. JL Patton UFJ Pardiñas G. Delía Rodents. The University of Chicago Press London and Chicago, 2015;818–876.

    Google Scholar 

  • Bogacka I, Paukszto Ł, Jastrzębski JP, Czerwińska J, Chojnowska K, Kamińska B, Kurzyńska A, Smolińska N, Giżejewski Z, Kamiński T. Seasonal differences in the testicular transcriptome profile of free-living European beavers (Castor fiber L.) determined by the RNA-Seq method. PLoS ONE. 2017;12:e0180323.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bosch OJ. Maternal aggression in rodents: brain oxytocin and vasopressin mediate pup defence. Philos Trans R Soc B Biol Sci. 2013;368(1631):20130085.

    Article  Google Scholar 

  • Breed WG, Leigh CM. Reproductive biology of an old endemic murid rodent of Australia, the Spinifex hop** mouse, Notomys alexis: adaptations for life in the arid zone. Integr Zool. 2011;6:321–33.

    Article  PubMed  Google Scholar 

  • Brewster J, Leon M. Relocation of the site of mother–young contact: maternal transport behavior in Norway rats. J Comp Physiol Psychol. 1980;94(1):69.

    Article  Google Scholar 

  • Bridges RS. A quantitative analysis of the roles of dosage, sequence, and duration of estradiol and progesterone exposure in the regulation of maternal behavior in the rat. Endocrinology. 1984;114(3):930–40.

    Article  CAS  PubMed  Google Scholar 

  • Bridges RS, Feder HH. Inhibitory effects of various progestins and deoxycorticosterone on the rapid onset of maternal behavior induced by ovariectomy-hysterectomy during late pregnancy in rats. Horm Behav. 1978;10(1):30–9.

    Article  CAS  PubMed  Google Scholar 

  • Bridges RS, Freemark MS. Human placental lactogen infusions into the medial preoptic area stimulate maternal behavior in steroid-primed, nulliparous female rats. Horm Behav. 1995;29(2):216–26.

    Article  CAS  PubMed  Google Scholar 

  • Bridges RS, Ronsheim PM. Prolactin (PRL) regulation of maternal behavior in rats: bromocriptine treatment delays and PRL promotes the rapid onset of behavior. Endocrinology. 1990;126(2):837–48.

    Article  CAS  PubMed  Google Scholar 

  • Bridges RS, Russell DW. Steroidal interactions in the regulation of maternal behaviour in virgin female rats: effects of testosterone, dihydrotestosterone, oestradiol, progesterone and the aromatase inhibitor, 1, 4, 6-Androstatriene-3, 17-Dione. J Endocrinol. 1981;90(1):31–40.

    Article  CAS  PubMed  Google Scholar 

  • Bridges RS, Goldman BD, Bryant LP. Serum prolactin concentrations and the initiation of maternal behavior in the rat. Horm Behav. 1974;5(3):219–26.

    Article  CAS  PubMed  Google Scholar 

  • Bridges RS, Rosenblatt JS, Feder HH. Serum progesterone concentrations and maternal behavior in rats after pregnancy termination: behavioral stimulation after progesterone withdrawal and inhibition by progesterone maintenance. Endocrinology. 1978;102(1):258–67.

    Article  CAS  PubMed  Google Scholar 

  • Bridges RS, DiBiase R, Loundes DD, Doherty PC. Prolactin stimulation of maternal behavior in female rats. Science. 1985;227(4688):782–4.

    Article  CAS  PubMed  Google Scholar 

  • Bridges RS, Numan M, Ronsheim PM, Mann PE, Lupini CE. Central prolactin infusions stimulate maternal behavior in steroid-treated, nulliparous female rats. Proc Natl Acad Sci. 1990;87(20):8003–7.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bridges RS, Robertson MC, Shiu RP, Sturgis JD, Henriquez BM, Mann PE. Central lactogenic regulation of maternal behavior in rats: steroid dependence, hormone specificity, and behavioral potencies of rat prolactin and rat placental lactogen I. Endocrinology. 1997;138(2):756–63.

    Article  CAS  PubMed  Google Scholar 

  • Broadbooks HE. Tree nesting and maternal behavior of chipmunks. Southwest Nat. 1977;22:154–5.

    Article  Google Scholar 

  • Brooks PL, Vella ET, Wynne-Edwards KE. Dopamine agonist treatment before and after the birth reduces prolactin concentration but does not impair paternal responsiveness in Djungarian hamsters, Phodopus campbelli. Horm Behav. 2005;47(3):358–66.

    Article  CAS  PubMed  Google Scholar 

  • Brown LN. Breeding Biology of the Pocket Gopher (Geomys pinetis) in Southern Florida. Am Midl Nat. 1971;85:45–53.

    Article  Google Scholar 

  • Brown RE. Hormonal and experiential factors influencing parental behaviour in male rodents: an integrative approach. Behav Process. 1993;30:1–27.

    Article  CAS  Google Scholar 

  • Brown RE, Murdoch T, Murphy PR, Moger WH. Hormonal responses of male gerbils to stimuli from their mate and pups. Horm Behav. 1995;29:474–91.

    Article  CAS  PubMed  Google Scholar 

  • Brown RS, Aoki M, Ladyman SR, Phillipps HR, Wyatt A, Boehm U, Grattan DR. Prolactin action in the medial preoptic area is necessary for postpartum maternal nursing behavior. Proc Natl Acad Sci. 2017;114(40):10779–84.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buntin JD, Jaffe S, Lisk RD. Changes in responsiveness to newborn pups in pregnant, nulliparous golden hamsters. Physiol Behav. 1984;32(3):437–9.

    Article  CAS  PubMed  Google Scholar 

  • Burgin CJ, Colella JP, Kahn PL, Upham NS. How many species of mammals are there?. Journal of Mammalogy, 2018;99(1):1–14.

    Google Scholar 

  • Burton M, Burton R. International wildlife encyclopedia, vol. 1. 3rd ed. Tarrytown: Marshall Cavendish; 2002.

    Google Scholar 

  • Busher P. Chapter 24. Social organization and monogamy in the beaver. In: Rodent societies. Chicago: University of Chicago Press; 2008.

    Google Scholar 

  • Butterworth BB. Parental relations and the behavior of juvenile kangaroo rats (Dipodomys) in captivity. Southwest Nat. 1964;8:213–20.

    Article  Google Scholar 

  • Camín S. Gestation, maternal behaviour, growth and development in the subterranean caviomorph rodent Ctenomys mendocinus (Rodentia, Hystricognathi, Ctenomyidae) Animal Biology. 2010;60(1):79–95.

    Google Scholar 

  • Camp CL. Excavations of burrows of the rodent aplodontia: with observations on the habits of the animal, vol. 17. Berkeley: University of California Press; 1918.

    Google Scholar 

  • Campo DH, Caraballo DA, Cassini GH, Lucero SO, Teta P. Integrative taxonomy of extant maras supports the recognition of the genera Pediolagus and Dolichotis within the Dolichotinae (Rodentia, Caviidae). J Mammal. 2020;101(3):817–34.

    Article  Google Scholar 

  • Carleton MD, Musser GG. Order Rodentia. In: Wilson DE, Reeder DM, editors. Mammal species of the world: a taxonomic and geographic reference. Baltimore: Johns Hopkins University Press; 2005. p. 745–52.

    Google Scholar 

  • Champagne F, Diorio J, Sharma S, Meaney MJ. Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc Natl Acad Sci. 2001;98(22):12736–41.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Champagne FA, Weaver IC, Diorio J, Sharma S, Meaney MJ. Natural variations in maternal care are associated with estrogen receptor α expression and estrogen sensitivity in the medial preoptic area. Endocrinology. 2003;144(11):4720–4.

    Article  CAS  PubMed  Google Scholar 

  • Champagne F, Chretien P, Stevenson CW, Zhang TY, Gratton A, Meaney MJ. Variations in nucleus accumbens dopamine associated with individual differences in maternal behavior in the rat. J Neurosci. 2004;24(17):4113–23.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Champagne FA, Curley JP, Keverne EB, Bateson PP. Natural variations in postpartum maternal care in inbred and outbred mice. Physiol Behav. 2007;91(2–3):325–34.

    Article  CAS  PubMed  Google Scholar 

  • Chen PB, Hu RK, Wu YE, Pan L, Huang S, Micevych PE, Hong W. Sexually dimorphic control of parenting behavior by the medial amygdala. Cell. 2019;176:1206–1221.e18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chojnowska K, Czerwinska J, Kaminski T, Kaminska B, Panasiewicz G, Kurzynska A, Bogacka I. Sex- and seasonally related changes in plasma gonadotropins and sex steroids concentration in the European beaver (Castor fiber). Eur J Wildl Res. 2015;61:807–11.

    Article  Google Scholar 

  • Chojnowska K, Czerwinska J, Kaminski T, Kaminska B, Kurzynska A, Bogacka I. Leptin plasma concentrations, leptin gene expression, and protein localization in the hypothalamic-pituitary-gonadal and hypothalamic-pituitary-adrenal axes of the European beaver (Castor fiber). Theriogenology. 2017;87:266–75.

    Article  CAS  PubMed  Google Scholar 

  • Clark MM, Galef BG. A testosterone-mediated trade-off between parental and sexual effort in male mongolian gerbils (Meriones unguiculatus). J Comp Psychol Wash DC. 1999;1983(113):388–95.

    Article  Google Scholar 

  • Clutton-Brock TH. The evolution of parental care. Princeton: Princeton University Press; 1991.

    Book  Google Scholar 

  • Concannon P, Baldwin B, Tennant B. Serum progesterone profiles and corpora lutea of pregnant, postpartum, barren and isolated females in a laboratory colony of woodchucks (Marmota monax). Biol Reprod. 1984;30(4):945–51.

    Article  CAS  PubMed  Google Scholar 

  • Connior MB. Geomys bursarius (Rodentia: Geomyidae). Mamm Species. 2011;43:104–17.

    Article  Google Scholar 

  • Coster, P.M.C., Beard, K.C., Salem, M.J., Chaimanee, Y., Jaeger, JJ., 2015. New fossils from the Paleogene of central Libya illuminate the evolutionary history of endemic African anomaluroid rodents. Front Earth Sci https://doi.org/10.3389/feart.2015.00056.

  • Cramblet HM, Ridenhour RL. Parturition in Aplodontia. J Mammal. 1956;37(1):87–90.

    Article  Google Scholar 

  • Crowley WR. Neuroendocrine regulation of lactation and milk production. Compr Physiol. 2011;5(1):255–91.

    Google Scholar 

  • Czerwińska J, Chojnowska K, Kamiński T, Bogacka I, Panasiewicz G, Smolińska N, Kamińska B. Plasma-glucocorticoids and ACTH levels during different periods of activity in the European Beaver (Castor fiber L.). Folia Biol (Praha). 2015;63:229–34.

    Article  Google Scholar 

  • Czerwińska J, Chojnowska K, Kaminski T, Bogacka I, Smolinska N, Kaminska B. Prepro-orexin and orexin expression in the hypothalamic–pituitary–adrenal and hypothalamic–pituitary–gonadal axes of free-living Eurasian beavers (Castor fiber L.) depends on season. J Mammal. 2017;98:895–905.

    Article  Google Scholar 

  • Dantzer B, McAdam AG, Palme R, Humphries MM, Boutin S, Boonstra R. Maternal androgens and behaviour in free-ranging North American red squirrels. Anim Behav. 2011;81(2):469–79.

    Article  Google Scholar 

  • Davis WB, Ramsey RR, Arendale JM Jr. Distribution of pocket gophers (Geomys breviceps) in relation to soils. J Mammal. 1938;19:412–8.

    Article  Google Scholar 

  • Dawson MR, Marivaux L, Li C, Beard KC, Metais G. Laonastes and the “Lazarus Effect” in recent mammals. Science. 2006;311(5766):1456–8.

    Article  CAS  PubMed  Google Scholar 

  • Day CS, Galef BG. Pup cannibalism: one aspect of maternal behavior in golden hamsters. J Comp Physiol Psychol. 1977;91(5):1179.

    Article  Google Scholar 

  • de Jong TR, Chauke M, Harris BN, Saltzman W. From here to paternity: neural correlates of the onset of paternal behavior in California mice (Peromyscus californicus). Horm Behav. 2009;56:220–31.

    Article  PubMed  Google Scholar 

  • de Jong TR, Measor KR, Chauke M, Harris BN, Saltzman W. Brief pup exposure induces Fos expression in the lateral habenula and serotonergic caudal dorsal raphe nucleus of paternally experienced male California mice (Peromyscus californicus). Neuroscience. 2010;169:1094–104.

    Article  PubMed  Google Scholar 

  • de Jong TR, Harris BN, Perea-Rodriguez JP, Saltzman W. Physiological and neuroendocrine responses to chronic variable stress in male California mice (Peromyscus californicus): influence of social environment and paternal state. Psychoneuroendocrinology. 2013;38:2023–33.

    Article  PubMed  Google Scholar 

  • de Olmos JS, Heimer L. The concepts of the ventral striatopallidal system and extended amugdada. Ann N Y Acad Sci. 1999;877:1–32.

    Article  PubMed  Google Scholar 

  • de Sousa FL, Lazzari V, de Azevedo MS, de Almeida S, Sanvitto GL, Lucion AB, Giovenardi M. Progesterone and maternal aggressive behavior in rats. Behav Brain Res. 2010;212(1):84–9.

    Article  PubMed  Google Scholar 

  • Dewsbury DA, Hodges AW. Copulatory Behavior and Related Phenomena in Spiny Mice (Acomys cahirinus) and Hop** Mice (Notomys alexis). J Mammal. 1987;68:49–57.

    Article  Google Scholar 

  • Dinets V. First observations on the behavior of the flightless anomalure (Zenkerella insignis). Zoology. 2017;123:121–3.

    Article  PubMed  Google Scholar 

  • Doerr HK, Siegel HI, Rosenblatt JS. Effects of progesterone withdrawal and estrogen on maternal behavior in nulliparous rats. Behav Neural Biol. 1981;32(1):35–44.

    Article  CAS  PubMed  Google Scholar 

  • Droge MH. Maternal retrieval in the lactation thirteen-lined ground squirrel, Spermophilus tridecemlineatus. Doctoral dissertation, Texas Tech University; 1976.

    Google Scholar 

  • Ebensperger LA, Ramírez-Otarola N, León C, Ortiz ME, Croxatto HB. Early fitness consequences and hormonal correlates of parental behaviour in the social rodent, Octodon degus. Physiol Behav. 2010;101(4):509–17.

    Article  CAS  PubMed  Google Scholar 

  • Edwards PD, Arguelles DA, Mastromonaco GF, Holmes MM. Queen pregnancy increases group estradiol levels in cooperatively breeding naked mole-rats. Integr Comp Biol. 2021;61:1841–51.

    Article  CAS  PubMed  Google Scholar 

  • Eisenberg J. Mammals of the neotropics. Chicago: The University of Chicago Press; 1989.

    Google Scholar 

  • Eisennberg JF, Isaac DE. The reproduction of heteromyid rodents in captivity. J Mammal. 1963;44:61–7.

    Article  Google Scholar 

  • Elyada YM, Mizrahi A. Becoming a mother – circuit plasticity underlying maternal behavior. Curr Opin Neurobiol. 2015;35:49–56.

    Article  CAS  PubMed  Google Scholar 

  • Ermisch A, Barth T, Rühle HJ, Skopkova J, Hrbas P, Landgraf R. On the blood-brain barrier to peptides: accumulation of labelled vasopressin, DesGlyNH2-vasopressin and oxytocin by brain regions. Endocrinol Exp. 1985;19(1):29–37.

    CAS  PubMed  Google Scholar 

  • Exner C, Wehrend A, Hospes R, Einspanier A, Hoffmann B, Heldmaier G. Hormonal and behavioural changes during the mating season and pregnancy in Alpine marmots (Marmota marmota). Reproduction. 2003;126(6):775–82.

    Article  CAS  PubMed  Google Scholar 

  • Fahrbach SE, Pfaff DW. Effect of preoptic region implants of dilute estradiol on the maternal behavior of ovariectomized, nulliparous rats. Horm Behav. 1986;20(3):354–63.

    Article  CAS  PubMed  Google Scholar 

  • Fahrbach SE, Morrell JI, Pfaff DW. Oxytocin induction of short-latency maternal behavior in nulliparous, estrogen-primed female rats. Horm Behav. 1984;18(3):267–86.

    Article  CAS  PubMed  Google Scholar 

  • Fahrbach SE, Morrell JI, Pfaff DW. Possible role for endogenous oxytocin in estrogen-facilitated maternal behavior in rats. Neuroendocrinology. 1985;40(6):526–32.

    Article  CAS  PubMed  Google Scholar 

  • Fahrbach SE, Morrell JI, Pfaff DW. Effect of varying the duration of pre-test cage habituation on oxytocin induction of short-latency maternal behavior. Physiol Behav. 1986;37(1):135–9.

    Article  CAS  PubMed  Google Scholar 

  • Fang YY, Yamaguchi T, Song SC, Tritsch NX, Lin D. A hypothalamic midbrain pathway essential for driving maternal behaviors. Neuron. 2018;98(1):192–207.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Farida WR, Sari AP, Inayah N, Nugroho HA. Observations of behavioral development on common Porcupines (Hystrix brachyura) undergoing domestication. IOP Conf Ser Earth Environ Sci. 2019;308:012076.

    Article  Google Scholar 

  • Feldhamer GA, Drickamer LC, Vessey SH, Merritt JF. Population growth and regulation. In: Mammalogy: adaptation, diversity, and ecology, vol. 1999. Boston: WCB/McGraw-Hill; 1999. p. 406–16.

    Google Scholar 

  • Feldhamer GA, Rochelle JA, Rushton CD. Mountain beaver (Aplodontia rufa). In: Wild mammals of North America: biology, management, and conservation. Baltimore: Johns Hopkins; 2003. p. 179–87.

    Google Scholar 

  • Felton TM, Linton LN, Rosenblatt JS, Morrell JI. Estrogen implants in the lateral habenular nucleus do not stimulate the onset of maternal behavior in female rats. Horm Behav. 1999;35(1):71–80.

    Article  Google Scholar 

  • Ferkin MH. Similarities between female meadow voles mating during post-partum oestrus and raising two concurrent litters and females raising only one litter. Reprod Fertil Dev. 2006;18(7):751–6.

    Article  PubMed  Google Scholar 

  • Fleischer S, Kordower JH, Kaplan B, Dicker R, Smerling R, Ilgner J. Olfactory bulbectomy and gender differences in maternal behaviors of rats. Physiol Behav. 1981;26:957–9.

    Article  CAS  PubMed  Google Scholar 

  • Fleming AS, Walsh C. Neuropsychology of maternal behavior in the rat: c-fos expression during mother-litter interactions. Psychoneuroendocrinology. 1994;19(5–7):429–43.

    Article  CAS  PubMed  Google Scholar 

  • Fleming AS, Cheung U, Myhal N, Kessler Z. Effects of maternal hormones on “timidity” and attraction to pup-related odors in female rats. Physiol Behav. 1989;46(3):449–53.

    Article  CAS  PubMed  Google Scholar 

  • Fleming AS, Corter C, Franks P, Surbey M, Schneider B, Steiner M. Postpartum factors related to mother’s attraction to newborn infant odors. Dev Psychobiol. 1993;26(2):115–32.

    Article  CAS  PubMed  Google Scholar 

  • Fokidis HB, Risch TS. The burden of motherhood: gliding locomotion in mammals influences maternal reproductive investment. J Mammal. 2008;89(3):617–25.

    Article  Google Scholar 

  • Foreman D, Garris D. Plasma progesterone levels and corpus luteum morphology in the female prairie dog (Cynomys ludovicianus). Gen Comp Endocrinol. 1984;55(2):315–22.

    Article  CAS  PubMed  Google Scholar 

  • Fowler CD, Johnson F, Wang Z. Estrogen regulation of cell proliferation and distribution of estrogen receptor-alpha in the brains of adult female prairie and meadow voles. J Comp Neurol. 2005;489:166–79.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fraser EJ, Shah NM. Complex chemosensory control of female reproductive behaviors. PLoS One. 2014;9:e90368.

    Article  PubMed  PubMed Central  Google Scholar 

  • Friedman MI, Bruno JP, Alberts JR. Physiological and behavioral consequences in rats of water recycling during lactation. J Comp Physiol Psychol. 1981;95(1):26.

    Article  CAS  PubMed  Google Scholar 

  • Fuchs T, Iacobucci P, MacKinnon KM, Panksepp J. Infant-mother recognition in a social rodent (octodon degus). J Comp Psychol. 2010;124(2):166–75.

    Article  PubMed  Google Scholar 

  • Gallagher JM, Nephew BC, Poirier G, King JA, Bridges RS. Estrogen receptor-alpha knockouts and maternal memory in nulliparous rats. Horm Behav. 2019;110:40–5.

    Article  CAS  PubMed  Google Scholar 

  • Garland HO, Atherton JC, Baylis C, Morgan MRA, Milne CM. Hormone profiles for progesterone, oestradiol, prolactin, plasma renin activity, aldosterone and corticosterone during pregnancy and pseudopregnancy in two strains of rat: correlation with renal studies. J Endocrinol. 1987;113(3):435–44.

    Article  CAS  PubMed  Google Scholar 

  • George W. Reproduction in female gundis (Rodentia: Ctenodactylidae). J Zool. 1978;185:57–71.

    Article  Google Scholar 

  • Ghiraldi LL, Svare B. Postpubertal isolation decreases infanticide and elevates parental care in C57BL/6J male mice. Physiol Behav. 1986;36:59–62.

    Article  CAS  PubMed  Google Scholar 

  • Gibori G, Sridaran R. Sites of androgen and estradiol production in the second half of pregnancy in the rat. Biol Reprod. 1981;24(2):249–56.

    Article  CAS  PubMed  Google Scholar 

  • Giordano AL, Ahdieh HB, Mayer AD, Siegel HI, Rosenblatt JS. Cytosol and nuclear estrogen receptor binding in the preoptic area and hypothalamus of female rats during pregnancy and ovariectomized, nulliparous rats after steroid priming: correlation with maternal behavior. Horm Behav. 1990;24(2):232–55.

    Article  CAS  PubMed  Google Scholar 

  • Glasper ER, Hyer MM, Katakam J, Harper R, Ameri C, Wolz T. Fatherhood contributes to increased hippocampal spine density and anxiety regulation in California mice. Brain Behav. 2016;6.

    Google Scholar 

  • González-Mariscal G, Melo AI. Neuroscience in the 21st century. New York: Springer Science and media; 2013.

    Google Scholar 

  • Gosling LM, Baker SJ. Planning and monitoring an attempt to eradicate coypus from Britain. Symp Zool Soc Lond. 1987;58:99–113.

    Google Scholar 

  • Grattan DR. 60 years of neuroendocrinology: the hypothalamo-prolactin axis. J Endocrinol. 2015;226(2):T101–22.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gréco B, Lubbers LS, Blaustein JD. Estrogen receptor β messenger ribonucleic acid expression in the forebrain of proestrous, pregnant, and lactating female rats. Endocrinology. 2003;144(5):1869–75.

    Article  PubMed  Google Scholar 

  • Grieb ZA, Tierney SM, Lonstein JS. Postpartum inhibition of ovarian steroid action increases aspects of maternal caregiving and reduces medial preoptic area progesterone receptor expression in female rats. Horm Behav. 2017;96:31–41.

    Article  CAS  PubMed  Google Scholar 

  • Grieb ZA, Vitale EM, Morrell JI, Lonstein JS, Pereira M. Decreased mesolimbic dopaminergic signaling underlies the waning of maternal caregiving across the postpartum period in rats. Psychopharmacology. 2020;237(4):1107–19.

    Article  CAS  PubMed  Google Scholar 

  • Groenewegen HJ, Berendse HW, Haber SN. Organization of the output of the ventral striatopallidal system in the rat: ventral pallidal efferents. Neuroscience. 1993;57(1):113–42.

    Article  CAS  PubMed  Google Scholar 

  • Gromov V. Interactions in family pairs and parental care in captive steppe lemming (Lagurus lagurus). Contemp Probl Ecol. 2010;3:133–9.

    Article  Google Scholar 

  • Gromov VS. Paternal care in rodents: Ultimate causation and proximate mechanisms. Russ J Theriol. 2020;19:1–20.

    Article  Google Scholar 

  • Grota LJ, Eik-Nes KB. Plasma progesterone concentrations during pregnancy and lactation in the rat. J Reprod Fertil. 1967;13(1):83–91.

    Google Scholar 

  • Grota LJ, Ader R. Continuous recording of maternal behaviour in Rattus norvegicus. Anim Behav. 1969;17(4):722–9.

    Article  Google Scholar 

  • Gubernick DJ. A maternal chemosignal maintains paternal behaviour in the biparental california mouse, Peromyscus californicus. Anim Behav. 1990;39:936–42.

    Article  Google Scholar 

  • Gubernick DJ, Alberts JR. Postpartum maintenance of paternal behaviour in the biparental California mouse, Peromyscus californicus. Anim Behav. 1989;37:656–64.

    Article  Google Scholar 

  • Gubernick DJ, Nelson RJ. Prolactin and paternal behavior in the biparental California mouse, Peromyscus californicus. Horm Behav. 1989;23:203–10.

    Article  CAS  PubMed  Google Scholar 

  • Guimarães DA, Ohashi OM, Singh M, Vale W. Profile of plasmatic progesterone on pregnancy, and the postpartum estrus of Dasyprocta prymnolopha (Rodentia: Dasyproctidae). Rev Biol Trop. 2016;64(4):1519–26.

    Article  PubMed  Google Scholar 

  • Guoynes C, Marler C. Paternal behavior from a neuroendocrine perspective. Neurosci: Oxf. Res. Encycl; 2020.

    Book  Google Scholar 

  • Hansen S, Sodersten P, Eneroth P. Mechanisms regulating hormone release and the duration of dioestrus in the lactating rat. J Endocrinol. 1983;99(2):173–80.

    Article  CAS  PubMed  Google Scholar 

  • Hansen S, Harthon C, Wallin E, Lofberg L, Svensson K. The effects of 6-OHDA-induced dopamine depletions in the ventral or dorsal striatum on maternal and sexual behavior in the female rat. Pharmacol Biochem Behav. 1991;39:71–7.

    Article  CAS  PubMed  Google Scholar 

  • Hansen S, Bergvall AH, Nyiredi S. Interaction with pups enhances dopamine release in the ventral striatum of maternal rats: a microdialysis study. Pharmacol Biochem Behav. 1993;45(3):673–6.

    Article  CAS  PubMed  Google Scholar 

  • Hasler J, Banks E. Reproductive performance and growth in captive collared lemmings (Dicrostonyx groenlandicus). Can J Zool. 1975;53:777–87.

    Article  CAS  PubMed  Google Scholar 

  • Hayden P, Gambino JJ, Lindberg RG. Laboratory breeding of the little pocket mouse, Perognathus longimembris. J Mammal. 1966;47:412–23.

    Article  Google Scholar 

  • Hayes UL, De Vries GJ. Role of pregnancy and parturition in induction of maternal behavior in prairie voles (Microtus ochrogaster). Horm Behav. 2007;51(2):265–72.

    Article  PubMed  Google Scholar 

  • Hayes LD, Chesh AS, Castro RA, Tolhuysen LO, Burger JR, Bhattacharjee J, Ebensperger LA. Fitness consequences of group living in the degu Octodon degus, a plural breeder rodent with communal care. Anim Behav. 2009;78:131–9.

    Article  Google Scholar 

  • Hayssen V. Reproductive effort in squirrels: ecological, phylogenetic, allometric, and latitudinal patterns. J Mammal. 2008;89(3):582–606.

    Article  Google Scholar 

  • He Z, Zhang L, Hou W, Zhang X, Young LJ, Li L, Liu L, Ma H, Xun Y, Lv Z, Li Y, Jia R, Li J, Tai F. Paraventricular nucleus oxytocin subsystems promote active paternal behaviors in mandarin voles. J Neurosci. 2021;41:6699–713.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hennessy MB, Jenkins R. A descriptive analysis of nursing behavior in the guinea pig (Cavia porcellus). J Comp Psychol. 1994;108(1):23.

    Article  CAS  PubMed  Google Scholar 

  • Herrera EA, Salas V, Congdon ER, Corriale MJ, Tang-Martinez Z. Capybara social structure and dispersal patterns: variations on a theme. J Mammal. 2011;92(1):12–20.

    Article  Google Scholar 

  • Hickman GC. The maternal behavior of a Mexican pocket gopher (Pappogeomys castanops). Southwest Nat. 1975;20:142–4.

    Article  Google Scholar 

  • Holekamp KE, Talamantes F. Seasonal variation in circulating testosterone and oestrogens of wild-caught California ground squirrels (Spermophilus beecheyi). Reproduction. 1991;93(2):415–25.

    Article  CAS  Google Scholar 

  • Holekamp KE, Nunes S, Talamantes F. Patterns of progesterone secretion in free-living California ground squirrels (Spermophilus beecheyi). Biol Reprod. 1988;39(5):1051–9.

    Article  CAS  PubMed  Google Scholar 

  • Hoogland JL. The black-tailed prairie dog: social life of a burrowing mammal. Chicago: University of Chicago Press; 1995.

    Google Scholar 

  • Horrell ND, Hickmott PW, Saltzman W. Neural regulation of paternal behavior in mammals: sensory, neuroendocrine, and experiential influences on the paternal brain. SpringerLink. 2018:1–50.

    Google Scholar 

  • Hume JM, Wynne-Edwards KE. Castration reduces male testosterone, estradiol, and territorial aggression, but not paternal behavior in biparental dwarf hamsters (Phodopus campbelli). Horm Behav. 2005;48:303–10.

    Article  CAS  PubMed  Google Scholar 

  • Hume JM, Wynne-Edwards KE. Paternal responsiveness in biparental dwarf hamsters (Phodopus campbelli) does not require estradiol. Horm Behav. 2006;49:538–44.

    Article  CAS  PubMed  Google Scholar 

  • Hyer MM, Hunter TJ, Katakam J, Wolz T, Glasper ER. Neurogenesis and anxiety-like behavior in male California mice during the mate’s postpartum period. Eur J Neurosci. 2016;43:703–9.

    Article  CAS  PubMed  Google Scholar 

  • Hyer MM, Khantsis S, Venezia AC, Madison FN, Hallgarth L, Adekola E, Glasper ER. Estrogen-dependent modifications to hippocampal plasticity in paternal California mice (Peromyscus californicus). Horm Behav. 2017;96:147–55.

    Article  CAS  PubMed  Google Scholar 

  • Insel TR. Regional changes in brain oxytocin receptors post-partum: time-course and relationship to maternal behaviour. J Neuroendocrinol. 1990;2(4):539–45.

    Article  CAS  PubMed  Google Scholar 

  • Izquierdo G, Lacey EA. Effects of group size on nest attendance in the communally breeding colonial tuco-tuco (Ctenomys sociabilis). Mamm Biol. 2008;73:438–43.

    Article  Google Scholar 

  • Jarvis JU. Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science. 1981;212(4494):571–3.

    Article  CAS  PubMed  Google Scholar 

  • Jenkins PD, Kilpatrick CW, Robinson MF, Timmins RJ. Morphological and molecular investigations of a new family, genus and species of rodent (Mammalia: Rodentia: Hystricognatha) from Lao PDR. Systematics and Biodiversity. 2 (4): 419–454. Corrigendum: Volume 2(4): 419–454. Syst Biodivers. 2005 3(3):343.

    Google Scholar 

  • Jones JS, Wynne-Edwards KE. Paternal hamsters mechanically assist the delivery, consume amniotic fluid and placenta, remove fetal membranes, and provide parental care during the birth process. Horm Behav. 2000;37:116–25.

    Article  CAS  PubMed  Google Scholar 

  • Juana L, Bárbara V-G, Martín M-T, Agustín C, Guillermo R-B, Guadalupe O. Neither testosterone levels nor aggression decrease when the male Mongolian gerbil (Meriones unguiculatus) displays paternal behavior. Horm Behav. 2010;57:271–5.

    Article  CAS  PubMed  Google Scholar 

  • Kalinichev M, Rosenblatt JS, Nakabeppu Y, Morrell JI. Induction of c-fos-like and fosB-like immunoreactivity reveals forebrain neuronal populations involved differentially in pup-mediated maternal behavior in juvenile and adult rats. J Comp Neurol. 2000;416(1):45–78.

    Article  CAS  PubMed  Google Scholar 

  • Katz LF, Ball GF, Nelson RJ. Elevated Fos-like immunoreactivity in the brains of postpartum female prairie voles, Microtus ochrogaster. Cell Tissue Res. 1999;298(3):425–35.

    Article  CAS  PubMed  Google Scholar 

  • Kawamichi M, Kawamichi T. Maternal care and independence of young Siberian chipmunks. Honyurui Kagaku [Mammal Sci]. 1984;48:3–17.

    Google Scholar 

  • Kawamichi M. Nest structure dynamics and seasonal use of nests by Siberian chipmunks (Eutamias sibiricus). J Mammalogy 1989;71:44–57.

    Google Scholar 

  • Kawamichi T, Kawamichi M. Gestation period and litter size of Siberian chipmunk Eutamias sibiricus lineatus in Hokkaido, northern Japan. J Mammal Soc Jpn. 1993;18(2):105–9.

    Google Scholar 

  • Keeley T, Goodrowe KL, Graham L, Howell C, MacDonald SE. The reproductive endocrinology and behavior of Vancouver Island marmot (Marmota vancouverensis). Zoo Biol. 2012;31(3):275–90.

    Article  CAS  PubMed  Google Scholar 

  • Kelly AM, Hiura LC, Saunders AG, Ophir AG. Oxytocin neurons exhibit extensive functional plasticity due to offspring age in mothers and fathers. Integr Comp Biol. 2017;57(3):603–18.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kenagy GJ, Barnes BM. Environmental and endogenous control of reproductive function in the Great Basin pocket mouse Perognathus parvus. Biol Reprod. 1984;31:637–45.

    Article  CAS  PubMed  Google Scholar 

  • Kenagy GJ, Bartholomew GA. Seasonal reproductive patterns in five coexisting California desert rodent species. Ecol Monogr. 1985;55:372–96. https://doi.org/10.2307/2937128.

    Article  Google Scholar 

  • Kenkel WM, Paredes J, Yee JR, Pournajafi-Nazarloo H, Bales KL, Carter CS. Neuroendocrine and behavioural responses to exposure to an infant in male prairie voles. J Neuroendocrinol. 2012;24:874–86.

    Article  CAS  PubMed  Google Scholar 

  • Kenkel WM, Suboc G, Sue Carter C. Autonomic, behavioral and neuroendocrine correlates of paternal behavior in male prairie voles. Physiol Behav. 2014;128:252–9. https://doi.org/10.1016/j.physbeh.2014.02.006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kercmar J, Snoj T, Tobet SA, Majdic G. Gonadectomy prior to puberty decreases normal parental behavior in adult mice. Horm Behav. 2014;66:667–73. https://doi.org/10.1016/j.yhbeh.2014.09.007.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kinsley CH, Bridges RS. Morphine treatment and reproductive condition alter olfactory preferences for pup and adult male odors in female rats. Dev Psychobiol. 1990;23(4):331–47.

    Article  CAS  PubMed  Google Scholar 

  • Kinsley GH, Lambert KG. Reproduction-induced neuroplasticity: natural behavioural and neuronal alterations associated with the production and care of offspring. J Neuroendocrinol. 2008;20(4):515–25.

    Article  CAS  PubMed  Google Scholar 

  • Kirkpatrick B, Kim JW, Insel TR. Limbic system fos expression associated with paternal behavior. Brain Res. 1994a;658:112–8. https://doi.org/10.1016/S0006-8993(09)90016-6.

    Article  CAS  PubMed  Google Scholar 

  • Kirkpatrick B, Williams JR, Slotnick BM, Carter CS. Olfactory bulbectomy decreases social behavior in male prairie voles (M. ochrogaster). Physiol Behav. 1994b;55:885–9. https://doi.org/10.1016/0031-9384(94)90075-2.

    Article  CAS  PubMed  Google Scholar 

  • Kirkpatrick B, Carter CS, Newman SW, Insel TR. Axon-sparing lesions of the medial nucleus of the amygdala decrease affiliative behaviors in the prairie vole (Microtus ochrogaster): behavioral and anatomical specificity. Behav Neurosci. 1994c;108:501–13.

    Article  CAS  PubMed  Google Scholar 

  • Kleiman DG. Maternal behaviour of the green acouchi (Myoprocta pratti Pocock), a South American caviomorph rodent. Behaviour. 1972;43(1/4):48–84.

    Google Scholar 

  • Kober M, Trillmich F, Naguib M. Vocal mother-offspring communication in guinea pigs: females adjust maternal responsiveness to litter size. Front Zool. 2008;5:13.

    Article  PubMed  PubMed Central  Google Scholar 

  • Koch M. Immunocytochemical localization and quantitation of estrogen-binding cells in the male and female (virgin, pregnant, lactating) mouse brain. Brain Res. 1989;489(1):101–12.

    Article  CAS  PubMed  Google Scholar 

  • Kohl J, Babayan BM, Rubinstein ND, Autry AE, Marin-Rodriguez B, Kapoor V, Miyamishi K, Zweifel LS, Luo L, Uchida N, Dulac C. Functional circuit architecture underlying parental behaviour. Nature. 2018;556:326–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kölliker M. The evolution of parental care. New York: Oxford University Press; 2012.

    Google Scholar 

  • Kraus C, Trillmich F, Kunkele J. Reproduction and growth in a precocial small mammal, Cavia magna. J Mammal. 2005;86(4):763–72.

    Article  Google Scholar 

  • Kuroda KO, Meaney MJ, Uetani N, Fortin Y, Ponton A, Kato T. ERK-FosB signaling in dorsal MPOA neurons plays a major role in the initiation of parental behavior in mice. Mol Cell Neurosci. 2007;36(2):121–31.

    Article  CAS  PubMed  Google Scholar 

  • Lacey EA, Sherman PW. Social organization of naked mole-rat colonies: evidence for a division of labor. In: Sherman PW, Jarvis JUM, Alexander RD, editors. The biology of the naked mole-rat. Princeton: Princeton University Press; 1991. p. 275–337.

    Google Scholar 

  • Lacey EA, Wieczorek JR. Kinship in colonial tuco-tucos: evidence from group composition and population structure. Behav Ecol. 2004;15:988–96.

    Article  Google Scholar 

  • Lambert KG, Franssen CL, Hampton JE, Rzucidlo AM, Hyer MM, True M, Kaufman C, Bardi M. Modeling paternal attentiveness: distressed pups evoke differential neurobiological and behavioral responses in paternal and nonpaternal mice. Neuroscience. 2013;234:1–12.

    Article  CAS  PubMed  Google Scholar 

  • Lau BYB, Krishnan K, Huang ZJ, Shea SD. Maternal experience-dependent cortical plasticity in mice is circuit- and stimulus-specific and requires MECP2. J Neurosci. 2020;40:1964–19.

    Article  Google Scholar 

  • Laurie EMO, Goodrich ES. The reproduction of the house-mouse (Mus musculus) living in different environments. Proc R Soc Lond Ser B Biol Sci. 1946;133:248–81.

    CAS  Google Scholar 

  • Lee AW, Brown RE. Medial preoptic lesions disrupt parental behavior in both male and female California mice (Peromyscus californicus). Behav Neurosci. 2002;116:968–75.

    Article  PubMed  Google Scholar 

  • Lee AW, Brown RE. Comparison of medial preoptic, amygdala, and nucleus accumbens lesions on parental behavior in California mice (Peromyscus californicus). Physiol Behav. 2007;92:617–28. https://doi.org/10.1016/j.physbeh.2007.05.008.

    Article  CAS  PubMed  Google Scholar 

  • Lee A, Clancy S, Fleming AS. Mother rats bar-press for pups: effects of lesions of the MPOA and limbic sites on maternal behavior and operant responding for pup reinforcement. Behav Brain Res. 2000;108:215–31.

    CAS  PubMed  Google Scholar 

  • Li Y, Lian Z, Wang B, Tai F, Wu R, Hao P, Qiao X. Natural variation in paternal behavior is associated with central estrogen receptor alpha and oxytocin levels. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2015;201:285–93.

    Article  CAS  PubMed  Google Scholar 

  • Lima SGC, Sousa-Lima RS, Tokumaru RS, Nogueira-Filho SLG, Nogueira SSC. Vocal complexity and sociality in spotted paca (Cuniculus paca). PLoS ONE. 2018;13(1):e0190961.

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu RC, Linden JF, Schreiner CE. Improved cortical entrainment to infant communication calls in mothers compared with virgin mice. Eur J Neurosci. 2006;23:3087–97.

    Article  PubMed  Google Scholar 

  • Lonstein JS. Effects of dopamine receptor antagonism with haloperidol on nurturing behavior in the biparental prairie vole. Pharmacol Biochem Behav. 2002;74:11–9.

    Article  CAS  PubMed  Google Scholar 

  • Lonstein JS, De Vries GJ. Comparison of the parental behavior of pair-bonded female and male prairie voles (Microtus ochrogaster). Physiol Behav. 1999;66:33–40.

    Article  CAS  PubMed  Google Scholar 

  • Lonstein JS, De Vries GJ. Influence of gonadal hormones on the development of parental behavior in adult virgin prairie voles (Microtus ochrogaster). Behav Brain Res. 2000;114:79–87. https://doi.org/10.1016/S0166-4328(00)00192-3.

    Article  CAS  PubMed  Google Scholar 

  • Lonstein JS, De Vries GJ. Social influences on parental and nonparental responses toward pups in virgin female prairie voles (Microtus ochrogaster). J Comp Psychol. 2001;115(1):53–61.

    Article  CAS  PubMed  Google Scholar 

  • Lonstein JS, Gammie SC. Sensory, hormonal, and neural control of maternal aggression in laboratory rodents. Neurosci Biobehav Rev. 2002;26(8):869–88.

    Article  PubMed  Google Scholar 

  • Lonstein JS, Gréco B, De Vries GJ, Stern JM, Blaustein JD. Maternal behavior stimulates c-fos activity within estrogen receptor alpha-containing neurons in lactating rats. Neuroendocrinology. 2000;72(2):91–101.

    Article  CAS  PubMed  Google Scholar 

  • Lonstein JS, Pereira M, Morrell JI, Marler CA. Parenting behavior. In: Knobil and Neill’s physiology of reproduction. New York: Academic; 2015. p. 2371–437.

    Chapter  Google Scholar 

  • Lovejoy BP, Black HC. Growth and weight of the mountain beaver, Aplodontia rufa pacifica. J Mammal. 1974;55(2):364–9.

    Article  CAS  PubMed  Google Scholar 

  • Lucas BK, Ormandy CJ, Binart N, Bridges RS, Kelly PA. Null mutation of the prolactin receptor gene produces a defect in maternal behavior. Endocrinology. 1998;139(10):4102–7.

    Article  CAS  PubMed  Google Scholar 

  • Luis J, Cadena C, Zedillo B, Reyes J, Ramos G, Martínez M. Testosterone replacement induced paternal behaviour in the Mexican volcano mouse Neotomodon alstoni (Rodentia Muridae). Ethol Ecol Evol. 2012;24:275–83.

    Article  Google Scholar 

  • Ma E, Lau J, Grattan DR, Lovejoy DA, Wynne-Edwards KE. Male and female prolactin receptor mRNA expression in the brain of a biparental and a uniparental hamster, phodopus, before and after the birth of a litter. J Neuroendocrinol. 2005;17:81–90.

    Article  CAS  PubMed  Google Scholar 

  • Macbeth AH, Stepp JE, Lee HJ, Young WS III, Caldwell HK. Normal maternal behavior, but increased pup mortality, in conditional oxytocin receptor knockout females. Behav Neurosci. 2010;124(5):677.

    Article  PubMed  PubMed Central  Google Scholar 

  • Macdonald D. The encyclopedia of mammals. New York: Facts on File Publications; 1984.

    Google Scholar 

  • Macdonald DW, Herrera EA, Taber AB, Moreira JR. Social organization and resource use in capybaras and maras. Chapter 33. In: Wolff JO, Sherman PW, editors. Rodent societies: an ecological and evolutionary perspective. Chicago: University of Chicago Press; 2007. p. 393–402.

    Google Scholar 

  • Maggi A. Liganded and unliganded activation of estrogen receptor and hormone replacement therapies. Biochim Biophys Acta (BBA)-Mol Basis Dis. 2011;1812(8):1054–60.

    Article  CAS  Google Scholar 

  • Mann PE, Bridges RS. Prolactin receptor gene expression in the forebrain of pregnant and lactating rats. Mol Brain Res. 2002;105(1–2):136–45.

    Article  CAS  PubMed  Google Scholar 

  • Marin G, Pilastro A. Communally breeding dormice, Glis glis, are close kin. Anim Behav. 1994;47(6):1485–7.

    Article  Google Scholar 

  • Marlin BJ, Mitre M, D’amour JA, Chao MV, Froemke RC. Oxytocin enables maternal behaviour by balancing cortical inhibition. Nature. 2015;520(7548):499–504.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martin P. Movements and activities of the mountain beaver (Aplodontia rufa). J Mammal. 1971;52(4):717–23.

    Article  Google Scholar 

  • Martínez A, Ramos G, Martínez-Torres M, Nicolás L, Carmona A, Cárdenas M, Luis J. Paternal behavior in the Mongolian gerbil (Meriones unguiculatus): estrogenic and androgenic regulation. Horm Behav. 2015;71:91–5.

    Article  PubMed  Google Scholar 

  • Mattheij JA, Swarts HJ, van Mourik S. Plasma prolactin in the rat during suckling without prior separation from pups. Eur J Endocrinol. 1985;108(4):468–74.

    Article  CAS  Google Scholar 

  • Mayer AD, Rosenblatt JS. Prepartum changes in maternal responsiveness and nest defense in Rattus norvegicus. J Comp Psychol. 1984;98(2):177.

    Article  CAS  PubMed  Google Scholar 

  • McAdam AG, Boutin S, Sykes AK, Humphries MM. Life histories of female red squirrels and their contributions to population growth and lifetime fitness. Ecoscience. 2007;14(3):362–9.

    Article  Google Scholar 

  • McCarthy MM, vom Saal FS. Infanticide by virgin CF-1 and wild male house mice (Mus musculus): effects of age, prolonged isolation, and testing procedure. Dev Psychobiol. 1986;19:279–90.

    Article  CAS  PubMed  Google Scholar 

  • McFadyen-Ketchum SA, Porter RH. Transmission of food preferences in spiny mice (Acomys cahirinus) via nose-mouth interaction between mothers and weanlings.Behavioral Ecology and Sociobiology, 1989;24(1):59–62.

    Google Scholar 

  • McGuire B, Novak M. A comparison of maternal behaviour in the meadow vole (Microtus pennsylvanicus), prairie vole (M. ochrogaster) and pine vole (M. pinetorum). Anim Behav. 1984;32:1132–41.

    Article  Google Scholar 

  • McGuire B, Russell KD, Mahoney T, Novak M. The effects of mate removal on pregnancy success in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus). Biol Reprod. 1992;47:37–42.

    Article  CAS  PubMed  Google Scholar 

  • McGuire B, Vermeylen F, Bemis WE. Suckling behaviour in three species of voles. Behaviour. 2011;148:551–73.

    Article  Google Scholar 

  • McHenry JA, Otis JM, Rossi MA, Robinson JE, Kosyk O, Miller NW, McElligott ZA, Budygin EA, Rubinow DR, Stuber GD. Hormonal gain control of a medial preoptic area social reward circuit. Nat Neurosci. 2017;20(3):449–58.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meddle SL, Bishop VR, Gkoumassi E, van Leeuwen FW, Douglas AJ. Dynamic changes in oxytocin receptor expression and activation at parturition in the rat brain. Endocrinology. 2007;148(10):5095–104.

    Article  CAS  PubMed  Google Scholar 

  • Mertz L. New world porcupines. In: Grzimek B, editor. Thomson Gale’s Grzimek’s animal life encyclopedia, vol. 13. New York/Cincinnati/Chicago: Van Nostrand Reinhold Co; 2003.

    Google Scholar 

  • Miceli MO, Malsbury CW. Sagittal knife cuts in the near and far lateral preoptic area-hypothalamus disrupt maternal behaviour in female hamsters. Physiol Behav. 1982;28(5):856–67.

    Article  CAS  PubMed  Google Scholar 

  • Michener GR. Maternal behaviour in Richardson's ground squirrel, Spermophilus richardsonii richardsonii: retrieval of young by lactating females. Anim Behav. 1971;19(4):653–6.

    Article  Google Scholar 

  • Mikkelsen E, Lauridsen H, Nielsen PM, Qi H, Nørlinger T, Andersen MD, Uldbjerg N, Laustsen C, Sandager P, Pedersen M. The chinchilla as a novel animal model of pregnancy. R Soc Open Sci. 2017;4(4):161098.

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller A, Jentz E, Duncan C. Progestogen metabolites for use in pregnancy monitoring of 13-lined ground squirrels (Ictidomys tridecemlineatus). Reprod Fertil. 2021;2(2):81–8.

    Article  PubMed  PubMed Central  Google Scholar 

  • Mitra SW, Hoskin E, Yudkovitz J, Pear L, Wilkinson HA, Hayashi S, Pfaff DW, Ogawa S, Rohrer SP, Schaeffer JM, McEwen BS. Immunolocalization of estrogen receptor β in the mouse brain: comparison with estrogen receptor α. Endocrinology. 2003;144(5):2055–67.

    Article  CAS  PubMed  Google Scholar 

  • Mogenson GJ, Jones DL, Yim CY. From motivation to action: functional interface between the limbic system and the motor system. Prog Neurobiol. 1980;14:69–97.

    Article  CAS  PubMed  Google Scholar 

  • Mori E, Lovari S, Sforzi A, Romeo G, Pisani C, Massolo A, Fattorini L. Patterns of spatial overlap in a monogamous large rodent, the crested porcupine. Behav Process. 2014;107:112–8.

    Article  Google Scholar 

  • Mori E, Menchetti M, Lucherini M, Sforzi A, Lovari S. Timing of reproduction and paternal cares in the crested porcupine. Mamm Biol. 2016;81:345–9.

    Article  Google Scholar 

  • Morris DJ, Van Aarde RJ. Sexual behavior of the female porcupine Hystrix africaeaustralis. Horm Behav. 1985;19(4):400–12.

    Article  CAS  PubMed  Google Scholar 

  • Murakami G. Distinct effects of estrogen on mouse maternal behavior: the contribution of estrogen synthesis in the brain. PLoS One. 2016;11(3):e0150728.

    Article  PubMed  PubMed Central  Google Scholar 

  • Muul I. Intra-and inter-familial behaviour of Glaucomys volans (Rodentia) following parturition. Anim Behav. 1970;18:20–5.

    Article  CAS  PubMed  Google Scholar 

  • Naguib M, Kober M, Trillmich F. Mother is not like mother: concurrent pregnancy reduces lactating guinea pigs’ responsiveness to pup calls. Behav Process. 2010;83(1):79–81.

    Article  Google Scholar 

  • Naughton D. The natural history of Canadian mammals. Toronto: University of Toronto Press; 2012.

    Book  Google Scholar 

  • Neckers LM, Zarrow MX, Myers MM, Denenberg VH. Influence of olfactory bulbectomy and the serotonergic system upon intermale aggression and maternal behavior in the mouse. Pharmacol Biochem Behav. 1975;3:545–50. https://doi.org/10.1016/0091-3057(75)90170-7.

    Article  CAS  PubMed  Google Scholar 

  • Nephew BC, Byrnes EM, Bridges RS. Vasopressin mediates enhanced offspring protection in multiparous rats. Neuropharmacology. 2010;58(1):102–6.

    Article  CAS  PubMed  Google Scholar 

  • Nimje PS, Tinnesand HV, Buesching C, Sæbø M, Senn H, Zedrosser A, Rosell F. Almost faithful: SNP markers reveal low levels of extra-pair paternity in the Eurasian beavers. PeerJ. 2019;7:e27866v1.

    Google Scholar 

  • Nishimori K, Takayanagi Y, Yoshida M, Kasahara Y, Young LJ, Kawamata M. New aspects of oxytocin receptor function revealed by knockout mice: sociosexual behaviour and control of energy balance. Prog Brain Res. 2008;170:79–90.

    Article  CAS  PubMed  Google Scholar 

  • Niswender GD, Juengel JL, McGuire WJ, Belfiore CJ, Wiltbank MC. Luteal function: the estrous cycle and early pregnancy. Biol Reprod. 1994;50(2):239–47.

    Article  CAS  PubMed  Google Scholar 

  • Nolte DL, Farley JP, Campbell DL, Epple GM, Mason JR. Potential repellents to prevent mountain beaver damage. Crop Prot. 1993;12(8):624–6.

    Article  CAS  Google Scholar 

  • Nowak RM. Walker’s Mammals of the World. 6th ed. Baltimore: Johns Hopkins University Press; 1999.

    Google Scholar 

  • Novak RM. 5th edn. The Johns Hopkins University Press; Baltimore, MD: 1991. Walker’s mammals of the world.

    Google Scholar 

  • Numan M. Progesterone inhibition of maternal behavior in the rat. Horm Behav. 1978;11(2):209–31.

    Article  CAS  PubMed  Google Scholar 

  • Numan M. The parental brain: mechanisms, development, and evolution. New York: Oxford University Press; 2020.

    Book  Google Scholar 

  • Numan M, Stolzenberg DS. Medial preoptic area interactions with dopamine neural systems in the control of the onset and maintenance of maternal behavior in rats. Front Neuroendocrinol. 2009;30(1):46–64.

    Article  CAS  PubMed  Google Scholar 

  • Numan M, Rosenblatt JS, Komisaruk BR. Medial preoptic area and onset of maternal behavior in the rat. J Comp Physiol Psychol. 1977;91(1):146.

    Article  CAS  PubMed  Google Scholar 

  • Numan M, Roach JK, del Cerro MCR, Guillamón A, Segovia S, Sheehan TP, Numan MJ. Expression of intracellular progesterone receptors in rat brain during different reproductive states, and involvement in maternal behavior. Brain Res. 1999;830(2):358–71.

    Article  CAS  PubMed  Google Scholar 

  • Nunes S, Muecke EM, Ross HE, Bartholomew PA, Holekamp KE. Food availability affects behavior but not circulating gonadal hormones in maternal Belding’s ground squirrels. Physiol Behav. 2000;71(5):447–55.

    Article  CAS  PubMed  Google Scholar 

  • Nutt KJ. Genetic reconstruction of breeding patterns in gundis (Rodentia: Ctenodactylidae). Behav Ecol Sociobiol. 2007;61(11):1651–63.

    Article  Google Scholar 

  • Ogawa S, Eng V, Taylor J, Lubahn DB, Korach KS, Pfaff DW. Roles of estrogen receptor-α gene expression in reproduction-related behaviors in female mice. Endocrinology. 1998;139(12):5070–81.

    Article  CAS  PubMed  Google Scholar 

  • Ojasti J. Estudio biologico del chigüire o capibara. Caracas: Ed. Fondo Nacional de Investigaciones Agropecuarias; 1973.

    Google Scholar 

  • Okabe S, Tsuneoka Y, Takahashi A, Ooyama R, Watarai A, Maeda S, Honda Y, Nagasawa M, Mogi K, Nishimori K, Kuroda M. Pup exposure facilitates retrieving behavior via the oxytocin neural system in female mice. Psychoneuroendocrinology. 2017;79:20–30.

    Article  CAS  PubMed  Google Scholar 

  • Oliveras D, Novak M. A comparison of paternal behaviour in the meadow vole Microtus pennsylvanicus, the pine vole M. pinetorum and the prairie vole M. ochrogaster. Anim Behav. 1986;34:519–26.

    Article  Google Scholar 

  • Olson ER, Carlson MR, Ramanujam VMS, Sears L, Anthony SE, Anich PS, Ramon L, Hulstrand A, Jurewicz M, Gunnelson AS, Kohler AM, Martin JG. Vivid biofluorescence discovered in the nocturnal Springhare (Pedetidae). Sci Rep. 2021;11:4125.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ostwald R, Wilken K, Simons J, Highstone H, Cimino S, Shimondle S. Influence of photoperiod and partial contact on estrus in the desert pocket mouse, Perognathus penicillatus. Biol Reprod. 1972;7:1–8.

    Article  CAS  PubMed  Google Scholar 

  • Paco A. Repetitive DNA sequences in rodentia genomes. Its involvement in chromosome architecture reshuffling and in genome functionality. Doctoral thesis, Universidade de Trás-os-Montes e Alto Douro, Portugal; 2014.

    Google Scholar 

  • Parker KJ, Lee TM. Central vasopressin administration regulates the onset of facultative paternal behavior in Microtus pennsylvanicus (meadow voles). Horm Behav. 2001;39:285–94. https://doi.org/10.1006/hbeh.2001.1655.

    Article  CAS  PubMed  Google Scholar 

  • Pedersen CA, Boccia ML. Oxytocin antagonism alters rat dams' oral grooming and upright posturing over pups. Physiol Behav. 2003;80(2–3):233–41.

    Article  CAS  PubMed  Google Scholar 

  • Pedersen CA, Prange AJ. Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc Natl Acad Sci. 1979;76(12):6661–5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pedersen CA, Ascher JA, Monroe YL, Prange AJ. Oxytocin induces maternal behavior in virgin female rats. Science. 1982;216(4546):648–50.

    Article  CAS  PubMed  Google Scholar 

  • Pedersen CA, Caldwell JD, Johnson MF, Fort SA, Prange AJ Jr. Oxytocin antiserum delays onset of ovarian steroid-induced maternal behavior. Neuropeptides. 1985;6(2):175–82.

    Article  CAS  PubMed  Google Scholar 

  • Pedersen CA, Caldwell JD, Walker C, Ayers G, Mason GA. Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav Neurosci. 1994;108(6):1163.

    Article  CAS  PubMed  Google Scholar 

  • Pedersen CA, Vadlamudi SV, Boccia ML, Amico JA. Maternal behavior deficits in nulliparous oxytocin knockout mice. Genes Brain Behav. 2006;5(3):274–81.

    Article  CAS  PubMed  Google Scholar 

  • Peinke DM, Brown CR. Burrow utilization by springhares (Pedetes capensis) in the Eastern Cape. S Afr Afr Zool. 2005;40(1):37–44.

    Article  Google Scholar 

  • Perea-Rodriguez JP, Takahashi EY, Amador TM, Hao RC, Saltzman W, Trainor BC. Effects of reproductive experience on central expression of progesterone, oestrogen α, oxytocin and vasopressin receptor mRNA in male California mice (Peromyscus californicus). J Neuroendocrinol. 2015;27:245–52.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira M. Nonselective maternal bonding but pup recognition in the subterranean rodent Ctenomys pearsoni. J Comp Psychol. 2006;120(4):411–5.

    Article  PubMed  Google Scholar 

  • Pereira M, Ferreira A. Demanding pups improve maternal behavioral impairments in sensitized and haloperidol-treated lactating female rats. Behav Brain Res. 2006;175(1):139–48.

    Article  CAS  PubMed  Google Scholar 

  • Pereira M, Ferreira A. Neuroanatomical and neurochemical basis of parenting: dynamic coordination of motivational, affective and cognitive processes. Horm Behav. 2016;77:72–85.

    Article  CAS  PubMed  Google Scholar 

  • Pereira M, Morrell JI. The changing role of the medial preoptic area in the regulation of maternal behavior across the postpartum period: facilitation followed by inhibition. Behav Brain Res. 2009;205(1):238–48.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pereira M, Morrell JI. Functional map** of the neural circuitry of rat maternal motivation: effects of site-specific transient neural inactivation. J Neuroendocrinol. 2011;23(11):1020–35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pereira M, Seip KM, Morrell JI. Maternal motivation and its neural substrate across the postpartum period. In: Bridges RS, editor. The neurobiology of the parental mind. San Diego: Elsevier Academic Press; 2008. p. 39–59.

    Google Scholar 

  • Perry AN, Sue Carter C, Cushing BS. Effects of postnatal estrogen manipulations on juvenile alloparental behavior. Horm Behav. 2015;75:11–7. https://doi.org/10.1016/j.yhbeh.2015.07.019.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfeiffer EW. The reproductive cycle of the female mountain beaver. J Mammal. 1958;39(2):223–35.

    Article  Google Scholar 

  • Phifer-Rixey M, Nachman MW. Insights into mammalian biology from the wild house mouse Mus musculus. elife. 2015;4:e05959.

    Article  PubMed Central  Google Scholar 

  • Pi XJ, Grattan DR. Increased prolactin receptor immunoreactivity in the hypothalamus of lactating rats. J Neuroendocrinol. 1999;11(9):693–705.

    Article  CAS  PubMed  Google Scholar 

  • Pi X, Zhang B, Li J, Voogt JL. Promoter usage and estrogen regulation of prolactin receptor gene in the brain of the female rat. Neuroendocrinology. 2003;77(3):187–97.

    Article  CAS  PubMed  Google Scholar 

  • Pilastro A. Communal nesting between breeding females in a free-living population of fat dormouse (Glis glis L.). Ital J Zool. 1992;59(1):63–8.

    Google Scholar 

  • Pilastro A, Missiaglia E, Marin G. Age-related reproductive success in solitarily and communally nesting female dormice (Glis glis). J Zool. 1996;239(3):601–8.

    Article  Google Scholar 

  • Pizzimenti JJ, McClenaghan LR Jr. Reproduction, growth and development, and behavior in the Mexican prairie dog, Cynomys mexicanus (Merriam). Am Midl Nat. 1974;92:130–45.

    Article  Google Scholar 

  • Pose S, Zuluaga MJ, Ferreño M, Agrati D, Bedó G, Uriarte N. Raising overlap** litters: differential activation of rat maternal neural circuitry after interacting with newborn or juvenile pups. J Neuroendocrinol. 2019;31(9):e12701.

    Article  PubMed  Google Scholar 

  • Potapov MA, Zadubrovskaya IV, Zadubrovskii PA, Potapova OF, Evsikov VI. Mating systems in the steppe lemming (Lagurus lagurus) and narrow-skulled vole (Microtus gregalis) from the Northern Kulunda Steppe. Russ J Ecol. 2012;43:40–4.

    Article  Google Scholar 

  • Randall JA, Matocq MD. Why do kangaroo rats (Dipodomys spectabilis) footdrum at snakes? Behav Ecol. 1997;8:404–13. https://doi.org/10.1093/beheco/8.4.404.

    Article  Google Scholar 

  • Reburn CJ, Wynne-Edwards KE. Hormonal changes in males of a naturally biparental and a uniparental mammal. Horm Behav. 1999;35:163–76. https://doi.org/10.1006/hbeh.1998.1509.

    Article  CAS  PubMed  Google Scholar 

  • Reichman OJ. Behavior of desert heteromyids. Gt Basin Nat Mem. 1983:77–90.

    Google Scholar 

  • Reisbick S, Rosenblatt JS, Mayer AD. Decline of maternal behavior in the virgin and lactating rat. J Comp Physiol Psychol. 1975;89(7):722–32.

    Article  CAS  PubMed  Google Scholar 

  • Ribeiro AC, Musatov S, Shteyler A, Simanduyev S, Arrieta-Cruz I, Ogawa S, Pfaff DW. siRNA silencing of estrogen receptor-α expression specifically in medial preoptic area neurons abolishes maternal care in female mice. Proc Natl Acad Sci. 2012;109(40):16324–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rich ME, deCárdenas EJ, Lee HJ, Caldwell HK. Impairments in the initiation of maternal behavior in oxytocin receptor knockout mice. PLoS One. 2014;9(6):e98839.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rioja-Paradela TM, Scott-Morales LM, Cotera-Correa M, Estrada-Castillón E. Reproduction and behavior of the Mexican prairie dog (Cynomys mexicanus). Southwest Nat. 2008;53(4):520–3.

    Article  Google Scholar 

  • Risold PY, Thompson RH, Swanson LW. The structural organization of connections between hypothalamus and cerebral cortex. Brain Res Brain Res Rev. 1997;19;24(2-3):197–254.

    Google Scholar 

  • Rosenblatt JS. Nonhormonal basis of maternal behavior in the rat. Science. 1967;156(3781):1512–3.

    Article  CAS  PubMed  Google Scholar 

  • Rosenblatt JS. The development of maternal responsiveness in the rat. Am J Orthopsychiatry. 1969;39(1):36–56.

    Google Scholar 

  • Rosenblatt JS. Prepartum and postpartum regulation of maternal behaviour in the rat. CIBA Found Symp. 1975;33:17–37.

    Google Scholar 

  • Rosenblatt JS. Psychobiology of maternal behavior: Contributions to the clinical understanding of maternal behavior among humans. Acta Paediatrica. 1994;83:3–8.

    Google Scholar 

  • Rosenblatt JS, Siegel HI. Hysterectomy-induced maternal behavior pregnancy in the rat. J Comp Physiol Psychol. 1975;89(7):685.

    Article  CAS  PubMed  Google Scholar 

  • Rosenblatt JS, Hazelwood S, Poole J. Maternal behavior in male rats: effects of medial preoptic area lesions and presence of maternal aggression. Horm Behav. 1996;30:201–15. https://doi.org/10.1006/hbeh.1996.0025.

    Article  CAS  PubMed  Google Scholar 

  • Rosi MI, Puig S, Videla F, Cona MI, Roig VG. Ciclo reproductivo y estructura etaria de Ctenomys mendocinus (Rodentia, Ctenomyidae) del Piedemonte de Mendoza, Argentina. Ecologfa Austral 1996;6:87–93.

    Google Scholar 

  • Royle, NJ, Smiseth, PT, Kölliker, M. The Evolution of Parental Care. OUP Oxford; 2012.

    Google Scholar 

  • Rubin BS, Menniti FS, Bridges RS. Intracerebroventricular administration of oxytocin and maternal behavior in rats after prolonged and acute steroid pretreatment. Horm Behav. 1983;17(1):45–53.

    Article  CAS  PubMed  Google Scholar 

  • Ruf T, Fietz J, Schlund W, Bieber C. High survival in poor years: life history tactics adapted to mast seeding in the edible dormouse. Ecology. 2006;87(2):372–81.

    Article  CAS  PubMed  Google Scholar 

  • Russell RJ. Evolution and classification of the pocket gophers of the subfamily Geomyinae. 2012.

    Google Scholar 

  • Saltzman W, Ziegler TE. Functional significance of hormonal changes in mammalian fathers. J Neuroendocrinol. 2014;26:685–96. https://doi.org/10.1111/jne.12176.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saltzman W, Harris BN, De Jong TR, Perea-Rodriguez JP, Horrell ND, Zhao M, Andrew JR. Paternal care in biparental rodents: intra- and inter-individual variation. Integr Comp Biol. 2017;57 https://doi.org/10.1093/icb/icx047.

  • Sanyal MK. Secretion of progesterone during gestation in the rat. J Endocrinol. 1978;79(2):179–90.

    Article  CAS  PubMed  Google Scholar 

  • Sarli J, Lutermann H, Alagaili AN, Mohammed OB, Bennett NC. Seasonal reproduction in the Arabian spiny mouse, Acomys dimidiatus (Rodentia: Muridae) from Saudi Arabia: the role of rainfall and temperature. J Arid Environ. 2016;124:352–9. https://doi.org/10.1016/j.jaridenv.2015.09.008.

    Article  Google Scholar 

  • Schiavo JK, Valtcheva S, Bair-Marshall CJ, Song SC, Martin KA, Froemke RC. Innate and plastic mechanisms for maternal behaviour in auditory cortex. Nature. 2020;587:426–31.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schiml PA, Hennessy MB. Light-dark variation and changes across the lactational period in the behaviors of undisturbed mother and infant guinea pigs (Cavia porcellus). J Comp Psychol. 1990;104(3):283.

    Article  CAS  PubMed  Google Scholar 

  • Schneider JE, Wade GN. Effects of maternal diet, body weight and body composition on infanticide in Syrian hamsters. Physiol Behav. 1989;46(5):815–21.

    Article  CAS  PubMed  Google Scholar 

  • Schneider JS, Burgess C, Horton TH, Levine JE. Effects of progesterone on male-mediated infant-directed aggression. Behav Brain Res. 2009;199:340–4. https://doi.org/10.1016/j.bbr.2008.12.019.

    Article  CAS  PubMed  Google Scholar 

  • Schum JE, Wynne-Edwards KE. Estradiol and progesterone in paternal and non-paternal hamsters (Phodopus) becoming fathers: conflict with hypothesized roles. Horm Behav. 2005;47:410–8. https://doi.org/10.1016/j.yhbeh.2004.11.009.

    Article  CAS  PubMed  Google Scholar 

  • Schneider JS, Stone MK, Wynne-Edwards KE, Horton TH, Lydon J, O’Malley B, Levine JE. Progesterone receptors mediate male aggression toward infants. Proceedings of the National Academy of Sciences of the United States of America, 2003;100(5):2951–2956.

    Google Scholar 

  • Scott CJ, Tilbrook AJ, Simmons DM, Rawson JA, Chu S, Fuller PJ, Ing NH, Clarke IJ. The distribution of cells containing estrogen receptor-alpha (ERalpha) and ERbeta messenger ribonucleic acid in the preoptic area and hypothalamus of the sheep: comparison of males and females. Endocrinology. 2000;141(8):2951–62.

    Article  CAS  PubMed  Google Scholar 

  • Sever Z, Mendelssohn H. Copulation as a possible mechanism to maintain monogamy in porcupines, Hystrix indica. Anim Behav. 1988;36:1541–2.

    Article  Google Scholar 

  • Sever Z, Mendelssohn H. Paternal behavior in porcupines. Isr J Zool. 1989;36:172–3.

    Google Scholar 

  • Sherman PW, Braude S, Jarvis JUM. Litter sizes and mammary numbers of naked mole-rats: breaking the one-half rule. J Mammal. 1999;80(3):720–33.

    Article  Google Scholar 

  • Shilton CM, Brooks RJ. Paternal care in captive collared lemmings (Dicrostonyx richardsoni) and its effect on development of the offspring. Can J Zool. 1989;67:2740–5. https://doi.org/10.1139/z89-388.

    Article  Google Scholar 

  • Shughrue PJ, Lane MV, Merchenthaler I. Comparative distribution of estrogen receptor-α and-β mRNA in the rat central nervous system. J Comp Neurol. 1997;388(4):507–25.

    Article  CAS  PubMed  Google Scholar 

  • Siegel HI, Greenwald GS. Prepartum onset of maternal behavior in hamsters and the effects of estrogen and progesterone. Horm Behav. 1975;6(3):237–45.

    Article  CAS  PubMed  Google Scholar 

  • Siegel HI, Rosenblatt JS. Estrogen-induced maternal behavior in hysterectomized-ovariectomized virgin rats. Physiol Behav. 1975;14(4):465–71.

    Article  CAS  PubMed  Google Scholar 

  • Simerly RB, Swanson LW. The organization of neural inputs to the medial preoptic nucleus of the rat. J Comp Neurol. 1986;246:312–42.

    Article  CAS  PubMed  Google Scholar 

  • Simerly RB, Swanson LW, Chang C, Muramatsu M. Distribution of androgen and estrogen receptor mRNA-containing cells in the rat brain: an in situ hybridization study. J Comp Neurol. 1990;294(1):76–95.

    Article  CAS  PubMed  Google Scholar 

  • Smiley, KO, Brown, RSE, and Grattan, DR. Prolactin action in the brain is required for paternal care in the mouse. BioRxiv 2021. https://doi.org/10.1101/2021.12.30.474525.

  • Smiley, KO, Ladyman, SR, Gustafson, P, Grattan, DR, Brown, RSE. Neuroendocrinology and Adaptive Physiology of Maternal Care. In: Neuroendocrine Regulation of Behavior. Springer International Publishing, 2019;161–210.

    Google Scholar 

  • Smolen MJ, Genoways HH, Baker RJ. Demographic and Reproductive Parameters of the Yellow-Cheeked Pocket Gopher (Pappogeomys castanops). J Mammal. 1980;61:224–36. https://doi.org/10.2307/1380043.

    Article  Google Scholar 

  • Stagkourakis S, Smiley KO, Williams P, Kakadellis S, Ziegler K, Bakker J, Brown RSE, Harkany T, Grattan DR, Broberger C. A neuro-hormonal circuit for paternal behavior controlled by a hypothalamic network oscillation. Cell. 2020;182:960–75.e15.

    Article  Google Scholar 

  • Stern JM. Parturition influences initial pup preferences at later onset of maternal behavior in primiparous rats. Physiol Behav. 1985;35(1):25–31.

    Article  CAS  PubMed  Google Scholar 

  • Stern JM. Multisensory regulation of maternal behavior and masculine sexual behavior: a revised view. Neurosci Biobehav Rev. 1990;14(2):183–200.

    Article  PubMed  Google Scholar 

  • Stern JM. Somatosensation and maternal care in Norway rats. In: Advances in the study of behavior, vol. 25. London: Academic; 1996. p. 243–94.

    Google Scholar 

  • Stern JM, Johnson SK. Ventral somatosensory determinants of nursing behavior in Norway rats. I. Effects of variations in the quality and quantity of pup stimuli. Physiol Behav. 1990;47(5):993–1011.

    Article  CAS  PubMed  Google Scholar 

  • Stern JM, Siegel HI. Prolactin release in lactating, primiparous and multiparous thelectomized and maternal virgin rats exposed to pup stimuli. Biol Reprod. 1978;19(1):177–82.

    Article  CAS  PubMed  Google Scholar 

  • Stier CH, Mensah GA, Gall CF. Elevage d’aulacodes (Thryonomys swinderianus) pour la production de viande. World Anim Rev. 1991;69:44–9.

    Google Scholar 

  • Stolzenberg DS, Rissman EF. Oestrogen-independent, experience-induced maternal behaviour in female mice. J Neuroendocrinol. 2011;23(4):345–54.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sturgis JD, Bridges RS. N-Methyl-DL-aspartic acid lesions of the medial preoptic area disrupt ongoing parental behavior in male rats. Physiol Behav. 1997;62:305–10. https://doi.org/10.1016/S0031-9384(97)88985-8.

    Article  CAS  PubMed  Google Scholar 

  • Swanson LW. An autoradiographic study of the efferent connections of the preoptic region in the rat. J Comp Neurol 1976;167(2):227–256.

    Google Scholar 

  • Swerdlow NR, Koob GF. Lesions of the dorsomedial nucleus of the thalamus, medial prefrontal cortex and pedunculopontine nucleus: effects on locomotor activity mediated by nucleus accumbens-ventral pallidal circuitry. Brain Res. 1987;412(2):233–43.

    Article  CAS  PubMed  Google Scholar 

  • Syrůčková A, Saveljev EP, Frosch C, Durka W, Savelyev AA, Munclinger P. Genetic relationships within colonies suggest genetic monogamy in the Eurasian beaver (Castor fiber). Mammal Res. 2014;60:139–47.

    Article  Google Scholar 

  • Tachikawa KS, Yoshihara Y, Kuroda KO. Behavioral transition from attack to parenting in male mice: a crucial role of the vomeronasal system. J Neurosci. 2013;33:5120–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tait AJ, Pope GS, Johnson, E. Progesterone concentrations in peripheral plasma of non-pregnant and pregnant grey squirrels (Sciurus carolinensis). J Endocrinol. 1981;89(1):107–16.

    Article  CAS  PubMed  Google Scholar 

  • Taraborelli PA, Sassi PL, Dacar MA, Moreno P, Ojeda RA. Abrocoma schistacea (Rodentia: Abrocomidae). Mamm Species. 2015;47(921):45–50.

    Article  Google Scholar 

  • Tasse J. Maternal and paternal care in the Rock Cavy, Kerodon rupestris, a South American hystricomorph rodent. Zoo Biol. 1986;5:27–43.

    Article  Google Scholar 

  • Taya K, Greenwald GS. Peripheral blood and ovarian levels of sex steroids in the lactating rat. Endocrinol Jpn. 1982;29(4):453–9.

    Article  CAS  PubMed  Google Scholar 

  • Taya K, Sasamoto S. Initiation of follicular maturation and ovulation after removal of the litter from the lactating rat. J Endocrinol. 1980;87(3):393–400.

    Article  CAS  PubMed  Google Scholar 

  • Terkel J, Rosenblatt JS. Maternal behavior induced by maternal blood plasma injected into virgin rats. J Comp Physiol Psychol. 1968;65(3p1):479.

    Article  CAS  PubMed  Google Scholar 

  • Terkel J, Rosenblatt JS. Humoral factors underlying maternal behavior at parturition: cross transfusion between freely moving rats. J Comp Physiol Psychol. 1972;80(3):365.

    Article  CAS  PubMed  Google Scholar 

  • Thorington RW Jr, Ferrell KE. Squirrels: the animal answer guide. Baltimore: JHU Press; 2006.

    Google Scholar 

  • Timonin ME, Wynne-Edwards KE. Aromatase inhibition during adolescence reduces adult sexual and paternal behavior in the biparental dwarf hamster Phodopus campbelli. Horm Behav. 2008;54:748–57.

    Article  CAS  PubMed  Google Scholar 

  • Timonin ME, Cushing BS, Wynne-Edwards KE. In three brain regions central to maternal behaviour, neither male nor female Phodopus dwarf hamsters show changes in oestrogen receptor alpha distribution with mating or parenthood. J Neuroendocrinol. 2008;20:1301–9.

    Article  CAS  PubMed  Google Scholar 

  • Tomasco IH, Sánchez L, Lessa EP, Lacey EA. Genetic analyses suggest burrow sharing by río negro tuco-tucos (Ctenomys rionegrensis). Mastozool Neotrop. 2019;26(2):430–9.

    Article  Google Scholar 

  • Trainor BC, Marler CA. Testosterone, paternal behavior, and aggression in the monogamous California Mouse (Peromyscus californicus). Horm Behav. 2001;40:32–42.

    Article  CAS  PubMed  Google Scholar 

  • Trainor BC, Marler CA. Testosterone promotes paternal behaviour in a monogamous mammal via conversion to oestrogen. Proc R Soc Lond B Biol Sci. 2002;269:823–9.

    Article  CAS  Google Scholar 

  • Trainor BC, Bird IM, Alday NA, Schlinger BA, Marler CA. Variation in aromatase activity in the medial preoptic area and plasma progesterone is associated with the onset of paternal behavior. Neuroendocrinology. 2003;78:36–44.

    Article  CAS  PubMed  Google Scholar 

  • Tsuneoka Y, Maruyama T, Yoshida S, Nishimori K, Kato T, Numan M, Kuroda KO. Functional, anatomical, and neurochemical differentiation of medial preoptic area subregions in relation to maternal behavior in the mouse. J Comp Neurol. 2013;521(7):1633–63.

    Article  CAS  PubMed  Google Scholar 

  • Tsuneoka Y, Tokita K, Yoshihara C, Amano T, Esposito G, Huang AJ, Yu LM, Odaka Y, Shinozuka K, McHugh TJ, Kuroda KO. Distinct preoptic-BST nuclei dissociate paternal and infanticidal behavior in mice. EMBO J. 2015;34:2652–70.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uriarte N, Ferreira A, Rosa XF, Sebben V, Lucion AB. Overlap** litters in rats: effects on maternal behavior and offspring emotionality. Physiol Behav. 2008;93(4–5):1061–70.

    Article  CAS  PubMed  Google Scholar 

  • Uriarte N, Fernández MV, Agrati D, Zuluaga MJ, Ferreño M, Ferreira A. Maternal and affective behaviors of lactating rats reared in overlap** litters. J Physiol Paris. 2014;108(2-3):221–230.

    Google Scholar 

  • Uriarte N, Ferreño M, Méndez D, Nogueira J. Reorganization of perineuronal nets in the medial Preoptic Area during the reproductive cycle in female rats. Sci Rep. 2020;10:Article number: 5479.

    Article  Google Scholar 

  • van Aarde RJ, Potgieter HC. Circulating progesterone, progesterone-binding proteins and oestradiol-17 beta concentrations in the pregnant Cape porcupine, Hystrix africaeaustralis. J Reprod Fertil. 1986;76(2):561–7.

    Article  PubMed  Google Scholar 

  • Veenema AH, Neumann ID. Central vasopressin and oxytocin release: regulation of complex social behaviours. Prog Brain Res. 2008;170:261–76.

    Article  CAS  PubMed  Google Scholar 

  • Vinograd A, Fuchs-Shlomai Y, Stern M, Mukherjee D, Gao Y, Citri A, Davison I, Mizrahi A. Functional plasticity of odor representations during motherhood. Cell Rep. 2017;21(2):351–65.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Voloschin LM, Tramezzani JH. Milk ejection reflex linked to slow wave sleep in nursing rats. Endocrinology. 1979;105(5):1202–7.

    Article  CAS  PubMed  Google Scholar 

  • Vom Saal FS. Variation in infanticide and parental behavior in male mice due to prior intrauterine proximity to female fetuses: elimination by prenatal stress. Physiol Behav. 1983;30:675–81. https://doi.org/10.1016/0031-9384(83)90162-2.

    Article  CAS  PubMed  Google Scholar 

  • Vom Saal FS. Time-contingent change in infanticide and parental behavior induced by ejaculation in male mice. Physiol Behav. 1985;34:7–15. https://doi.org/10.1016/0031-9384(85)90069-1.

    Article  CAS  PubMed  Google Scholar 

  • Wagner CK, Morrell JI. In situ analysis of estrogen receptor mRNA expression in the brain of female rats during pregnancy. Mol Brain Res. 1995;33(1):127–35.

    Article  CAS  PubMed  Google Scholar 

  • Wagner CK, Morrell JI. Levels of estrogen receptor immunoreactivity are altered in behaviorally-relevant brain regions in female rats during pregnancy. Mol Brain Res. 1996;42(2):328–36.

    Article  CAS  PubMed  Google Scholar 

  • Wamboldt MZ, Insel TR. The ability of oxytocin to induce short latency maternal behavior is dependent on peripheral anosmia. Behav Neurosci. 1987;101(3):439.

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, De Vries GJ. Testosterone effects on paternal behavior and vasopressin immunoreactive projections in prairie voles (Microtus ochrogaster). Brain Res. 1993;631:156–60.

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Ferris CF, De Vries GJ. Role of septal vasopressin innervation in paternal behavior in prairie voles (Microtus ochrogaster). Proc Natl Acad Sci U S A. 1994a;91:400–4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Z, Smith W, Major DE, De Vries GJ. Sex and species differences in the effects of cohabitation on vasopressin messenger RNA expression in the bed nucleus of the stria terminalis in prairie voles (Microtus ochrogaster) and meadow voles (Microtus pennsylvanicus). Brain Res. 1994b;650:212–8. https://doi.org/10.1016/0006-8993(94)91784-1.

    Article  CAS  PubMed  Google Scholar 

  • Wang ZX, Liu Y, Young LJ, Insel TR. Hypothalamic vasopressin gene expression increases in both males and females postpartum in a biparental rodent. J Neuroendocrinol. 2000;12:111–20.

    Article  CAS  PubMed  Google Scholar 

  • Watarai A, Arai N, Miyawaki S, Okano H, Miura K, Mogi K, Kikusui T. Responses to pup vocalizations in subordinate naked mole-rats are induced by estradiol ingested through coprophagy of queen’s feces. PNAS. 2018;115(37):9264–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei YC, Wang SR, Jiao ZL, Zhang W, Lin JK, Li XY, Li SS, Zhang X, Xu XH. Medial preoptic area in mice is capable of mediating sexually dimorphic behaviors regardless of gender. Nat Commun. 2018;9(1):1–15.

    Article  Google Scholar 

  • Wight HM. Breeding habits and economic relations of the Dalles Pocket Gopher. J Mammal. 1930;11:40–8.

    Article  Google Scholar 

  • Wilson DE, Reeder DM. Mammal species of the world: a taxonomic and geographic reference. 2nd ed. Washington, DC/London: Smithsonian Institution Press; 1993.

    Google Scholar 

  • Witmer GW, Lowney M. Population biology and monitoring of the Cuban hutia at Guantanamo Bay, Cuba. Mammalia. 2007;71:115–21.

    Article  Google Scholar 

  • Wöhr M, Oddi D, D’Amato FR. Effect of altricial pup ultrasonic vocalization on maternal behavior. In: Handbook of behavioral neuroscience, vol. 19. Amsterdam: Elsevier; 2010. p. 159–66.

    Google Scholar 

  • Wood JE. Reproductive Pattern of the Pocket Gopher (Geomys breviceps brazensis). J Mammal. 1949;30:36–44. https://doi.org/10.2307/1375195.

    Article  CAS  PubMed  Google Scholar 

  • Wu Z, Autry AE, Bergan JF, Watabe-Uchida M, Dulac CG. Galanin neurons in the medial preoptic area govern parental behaviour. Nature. 2014;509:325–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yadav R, Haldar C. Variation in gonadal steroid and melatonin during gestation of a diurnal seasonal breeder Indian palm squirrel Funambulus pennanti. J Endocrinol Reprod. 2009;13(1):1–6.

    CAS  Google Scholar 

  • Yoshihara C, Numan M, Kuroda KO. Oxytocin and parental behaviors. In: Behavioral pharmacology of neuropeptides: oxytocin. Cham: Springer; 2017. p. 119–53.

    Chapter  Google Scholar 

  • Yuan W, Yang X-P, Yu P, Jia R, Tai F-D, Wei B, Liu X, Ma L-G. Different behavioral, neural and neuropeptide responses of fathers to their own and to alien pups in mandarin voles. J Comp Physiol A. 2017:1–13. https://doi.org/10.1007/s00359-017-1229-x.

  • Zhang GW, Shen L, Tao C, Jung AH, Peng B, Li Z, Zhang LI, Tao HW. Medial preoptic area antagonistically mediates stress-induced anxiety and parental behavior. Nat Neurosci. 2021;24(4):516–28.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Psychological and Brain Sciences, University of Massachusetts, Amherst, MA, USA

    Mariana Pereira

  2. Centre for Neuroendocrinology & Department of Anatomy, School of Biomedical Sciences, University of Otago, Dunedin, New Zealand

    Kristina O. Smiley

  3. Department of Psychology & Neuroscience Program, Michigan State University, East Lansing, MI, USA

    Joseph S. Lonstein

Authors
  1. Mariana Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kristina O. Smiley
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joseph S. Lonstein
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joseph S. Lonstein .

Editor information

Editors and Affiliations

  1. Center for Research in Animal Reproduction, CINVESTAV-Universidad Autonoma de Tlaxcala, Tlaxcala, Mexico

    Gabriela González-Mariscal

Rights and permissions

Reprints and permissions

Copyright information

© 2022 The Author(s), under exclusive license to Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Pereira, M., Smiley, K.O., Lonstein, J.S. (2022). Parental Behavior in Rodents. In: González-Mariscal, G. (eds) Patterns of Parental Behavior. Advances in Neurobiology, vol 27. Springer, Cham. https://doi.org/10.1007/978-3-030-97762-7_1

Download citation

Publish with us

Policies and ethics

Search

Navigation