Pair-bonding and parental care in cricetid rodents: a comparative study

• Autorzy: Gromov V. S.
• Języki publikacji: EN

Abstrakty

EN

The cricetid rodents (hamsters, voles, and gerbils) show substantial inter-specific variation in their social organization, mating strategies, and patterns of social behavior, including parental care. In the present study, behaviors related to pair-bonding and parental activities were evaluated in male–female pairs of six cricetid species (Cricetulus migratorius Pallas, 1773, Clethrionomys rutilus Pallas, 1779, Microtus arvalis Pallas, 1778, Microtus socialis Pallas, 1773, Lasiopodomys brandti Radde, 1852, and Meriones unguiculatus Milne-Edwards, 1867) observed under laboratory conditions. These species were chosen due to particular differences in their mating strategies and the spatial-and-ethological population structure (Types I–IV). The results of the study show that there is a pronounced tendency towards both reinforcement of pair-bonds and increasing rate of direct parental care, especially paternal one, when solitary or gregarious species (Types I and II—C. migratorius and C. rutilus) are compared with the ones living in family groups (Type III—M. arvalis and M. socialis and Type IV—L. brandti and M. unguiculatus). Parental investment of males is mainly related to additional tactile stimulation of infants. A high level of tactile stimulation of pups promotes an increase in subsequent paternal care and reinforcement of pair-bonding, and, conversely, a deficit of tactile stimulation negatively affects the development of paternal behavior and social relationships. Thus, tactile stimulation can be regarded as one of the proximate mechanisms of socialization that plays an essential role in the evolution of sociality, i.e., transition to a family-group mode of life in rodents.

Słowa kluczowe

EN

pair bonding; parental care; cricetid rodent; rodent; comparative study

• Wydawca: -
• Czasopismo: Acta Theriologica
• Rocznik: 2011
• Tom: 56
• Numer: 1
• Opis fizyczny: p.23-33,fig.,ref.

Twórcy

autor

Gromov V. S.

• A.N.Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, 33 Leninsky prosp., Moscow 119071, Russia

Bibliografia

• Ågren G, Zhou Q, Zhong W (1989) Ecology and social behaviour of Mongolian gerbils, Meriones unguiculatus, at Xilinhot, Inner Mongolia, China. Anim Behav 37:11–27. doi:10.​1016/​0003-3472(89)90002-X
• Armitage KB (1981) Sociality as a life-history tactic of ground squirrels. Oecologia 48:36–49. doi:10.​1007/​BF00346986
• Arnold W (1990a) The evolution of marmot sociality: I. Why disperse late? Behav Ecol Sociobiol 27:229–237
• Arnold W (1990b) The evolution of marmot sociality: II. Costs and benefits of joint hibernation. Behav Ecol Sociobiol 27:239–246
• Bridges RS, Zarrow MX, Goldman BD, Denenberg VH (1974) A developmental study of maternal responsiveness in the rat. Physiol Behav 12:149–151
• Brown RE, Matheison WB, Stapleton J, Neumann PE (1999) Maternal behavior in female C57BL/6J and DBA/2J inbred mice. Physiol Behav 67:599–605. doi:10.​1016/​S0031-9384(99)00109-2
• Carter CS, Getz LL (1993) Monogamy and prairie vole. Sci Am 268:100–106. doi:10.​1038/​scientificameric​an0693-100
• Clark MM, Desousa D, Vonk J, Galef BG (1997) Parenting and potency: alternative routes to reproductive success in male Mongolian gerbils. Anim Behav 54:635–642. doi:10.​1006/​anbe.​1997.​0468
• Cramer CP (1988) Experience during suckling increases weight and volume of rat hippocampus. Brain Res 470:151–155. doi:10.​1016/​0165-3806(88)90212-X
• Dewsbery DA (1985) Paternal behavior in rodents. Am Zool 25:841–852. doi:10.​1093/​icb/​25.​3.​841
• Dezhkin VV, D’jakov YuV, Safonov VG (1986) [European castor]. Agropromizdat, Moscow [in Russian]
• Eilam D, Smotherman WP (1998) How the neonatal rat gets to the nipple: common motor modules and their involvement in the expression of early motor behavior. Dev Psychobiol 32:57–66. doi:10.​1002/​(SICI)1098-2302(199801)32:​1<57:​:​AID-DEV7>3.​0.​CO;2-S
• Elwood RW (1975) Paternal and maternal behaviour in the Mongolian gerbil. Anim Behav 23:766–772. doi:10.​1016/​0003-3472(75)90104-9
• Elwood RW (1983) Paternal care in rodents. In: Elwood RW (ed) Paternal behaviour of rodents. Wiley, Chichester, pp 235–257
• Francis D, Diorio J, Liu D, Meany MJ (1999) Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286:1155–1158. doi:10.​1126/​science.​286.​5442.​1155
• Gonzalez A, Lovic V, Ward GR, Wainwright PE, Fleming AS (2001) Intergenerational effects of complete maternal deprivation and replacement stimulation on maternal behaviour and emotionality in female rats. Dev Psychobiol 38:11–32. doi:10.​1002/​1098-2302(2001)38:​1<11:​:​AID-DEV2>3.​0.​CO;2-B
• Gromov VS (2003) [Territorial structure and social organization in the Brandt vole (Lasiopodomys brandti) under semi-natural conditions]. Zool Zh 82:852–861 [in Russian with English summary]
• Gromov VS (2005a) [Types of the spatial-and-ethological population structure in rodents]. Zool Zh 84:1003–1014 [in Russian with English summary]
• Gromov VS (2005b) Parental care in captive Brandt vole (Lasiopodomys brandti). Russian J Theriol 4(2):137–145
• Gromov VS (2007) Parental care in captive social vole (Microtus socialis). Zool Zh 86:1389–1397 [in Russian with English summary]
• Gromov VS (2008) [The spatial-and-ethological structure of rodent populations]. KMK Press, Moscow [in Russian]
• Gromov VS (2009a) Parental care in captive red-backed vole (Clethrionomys rutilus). Cont Probl Ecol 2(3):11–18. doi:10.​1134/​S199542550903017​5
• Gromov VS (2009b) Interactions of partners in family pairs, care of the offspring, and the role of tactile stimulation in formation of parental behaviour of the Mongolian gerbil (Meriones unguiculatus) under laboratory conditions. Biol Bull 36(5):479–488. doi:10.​1134/​S106235900905008​2
• Gromov VS, Surov AV, Ryurikov GB (2006) Maternal care in captive grey hamster Cricetulus migratorius (Rodentia, Cricetidae). Russ J Theriol 5(2):73–77
• Gubernick DJ, Alberts JR (1987) The biparental care system of the California mouse, Peromyscus californicus. J Comp Psychol 101:169–177. doi:10.​1037/​0735-7036.​101.​2.​169
• Hartung TG, Dewsbury DA (1979) Paternal behavior of six species of muroid rodents. Behav Neural Biol 26:446–478. doi:10.​1016/​S0163-1047(79)91500-0
• Hofer MA (1978) Hidden regulatory processes in early social relationships. In: Bateson PPG, Klopfer PH (eds) Perspectives in ethology. Plenum Press, New York, pp 135–166
• Hofmann JE, McGuire B, Pizzuto TM (1989) Parental care in the sagebush vole (Lemmiscus curtatus). J Mammal 70:162–165. doi:10.​2307/​1381679
• Hutchison JB, Steimer T (1984) Androgen metabolism in the brain: behavioral correlates. Prog Brain Res 61:23–51. doi:10.​1016/​S0079-6123(08)64427-1
• Insel TR (1990) Oxytocin and maternal behaviour. In: Drasnegor NA, Bridges RS (eds) Mammalian parenting. Oxford, New York, pp 260–280. doi:10.​1111/​j.​1749-6632.​1992.​tb34350.​x
• Insel T (1997) A neurobiological basis of social attachment. Am J Psychiatry 154:726–735
• Kleiman DG (1977) Monogamy in mammals. Q Rev Biol 52:39–69. doi:10.​1086/​409721
• Libhaber N, Eilam D (2004) Parental investment in social voles varies and is relatively independent of litter size. J Mammal 85:748–755. doi:10.​1644/​BNS-011
• Liu D, Diorio J, Tannenbaum B et al (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277:1659–1662. doi:10.​1126/​science.​277.​5332.​1659
• Lonstein JS, De Vries GJ (1999) Comparison of the parental behaviour of pair-bonded female and male prairie voles (Microtus ochrogacter). Physiol Behav 66:33–40. doi:10.​1016/​S0031-9384(98)00270-4
• Lonstein JS, De Vries GJ (2000) Sex differences in the parental behavior of rodents. Neurosci Biobehav Rev 24:669–686. doi:10.​1016/​S0149-7634(00)00036-1
• McGuire B (1988) Effects of cross-fostering on parental behaviour of meadow voles (Microtus pennsylvanicus). J Mammal 69:332–341. doi:10.​2307/​1381383
• McGuire B (1997) Influence of father and pregnancy on maternal care in red-backed voles. J Mammal 78:839–849. doi:10.​2307/​1382942
• McGuire B, Novak M (1984) A comparison of maternal behaviour in the meadow vole (Mictotus pennsylvanicus), prairie vole (M. ochrogaster) and pine vole (M. pinetorum). Anim Behav 32:1132–1141. doi:10.​1016/​S0003-3472(84)80229-8
• McGuire B, Novak M (1986) Parental care and its relation to social organization in the montane vole. J Mammal 67:305–311
• Nelson E, Panksepp J (1998) Brain substrates of infant-mother attachment: contributions of opioids, oxytocin and norepinephrine. Neurosci Biobehav Rev 22:437–452. doi:10.​1016/​S0149-7634(97)00052-3
• Numan M (1994) Maternal behavior. In: Knobil E, Neill JD (eds) The physiology of reproduction. Raven Press, New York, pp 221–302
• Oliveras D, Novak M (1986) A comparison of paternal behavior in the meadow vole, Microtus pennsylvanicus, the pine vole, Microtus pinetorum, and prairie vole, Microtus ochrogaster. Anim Behav 34:519–526
• Post RM, Weiss SR et al (1998) Neural plasticity and emotional memory. Dev Psychopathol 10:829–855. doi:10.​1017/​S095457949800189​8
• Proulx G, Gilbert FF (1983) The ecology of the muskrat, Ondatra zibethicus, at Luther Marsh, Ontario. Can Field-Nat 97:377–390
• Reburn CJ, Winne-Edwards KE (1989) Hormonal changes in males of a naturally biparental and a uniparental mammal. Horm Behav 35:163–176. doi:10.​1006/​hbeh.​1998.​1509
• Roberts RL, Williams JR, Wang AK, Carter CS (1998) Cooperative breeding and monogamy in prairie voles: influence of the sire and geographic variation. Anim Behav 55:1131–1140. doi:10.​1006/​anbe.​1997.​0659
• Rosenblatt GS, Lehrman DS (1963) Maternal behaviour of the laboratory rat. In: Rheingold HL (ed) Maternal behaviour in mammals. Wiley, London, pp 8–57
• Rosenzweig MR, Bennet EL (1996) Psychobiology of plasticity: effects of training and experience on brain and behavior. Behav Brain Res 78:57–65. doi:10.​1016/​0166-4328(95)00216-2
• Rowell TE (1961) Maternal behaviour in non-lactating golden hamsters. Anim Behav 9:11–15
• Shilton CM, Brooks RJ (1989) Paternal care in captive collared lemmings (Dicrostonyx richardsoni) and its effect on development of the offspring. Can J Zool 67:2740–2745. doi:10.​1139/​z89-388
• Smorkatcheva AV (2003) Parental care in the captive mandarin vole, Lasiopodomys mandarinus. Can J Zool 81:1339–1345. doi:10.​1139/​z03-100
• Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. Plenum Press, New York
• Solomon NG (1993) Comparison of parental behaviour in male and female prairie voles (Microtus ochrogacter). Can J Zool 71:434–437. doi:10.​1139/​z93-061
• Svendsen GE (1980) Population parameters and colony composition of beaver (Castor canadensis) in southeast Ohio. Am Midl Nat 104:47–56. doi:10.​2307/​2424957
• Thomas JA, Birney EC (1979) Parental care and mating system of the prairie vole, Microtus ochrogaster. Behav Ecol Sociobiol 5:171–186. doi:10.​1007/​BF00293304
• Wang ZX, Insel TR (1996) Parental behavior in voles. Adv Study Behav 25:361–384. doi:10.​1016/​S0065-3454(08)60338-1
• Wilson SC (1982) Parent-young contact in prairie and meadow voles. J Mammal 63:300–305. doi:10.​2307/​1380642
• Wynne-Edwards KE (2001) Hormonal changes in mammalian fathers. Horm Behav 40:139–145. doi:10.​1006/​hbeh.​2001.​1699
• Xia X, Millar JS (1988) Paternal behavior by Peromyscus leucopus in enclosures. Can J Zool 66:1184–1187. doi:10.​1139/​z88-173
• Young LJ (1999) Oxytocin and vasopressin receptors and species-typical social behaviors. Horm Behav 36:212–221. doi:10.​1006/​hbeh.​1999.​1548
• Zorenko TA (1994) Ethology. In: The common vole: sibling species Microtus arvalis Pallas, 1779 and M. rossiaemeridionalis Ognev, 1924. Nauka Publ, Moscow, pp 289–297 [In Russian]

Identyfikatory

DOI

10.1007/s13364-010-0013-x