Patterns of Body Temperature, Activity, and Reproductive Behavior in a Tropical Murid Rodent, Arvicanthis niloticus

doi:10.1016/S0031-9384(97)00146-7

Physiology & Behavior

Volume 62, Issue 1, July 1997, Pages 91-96

https://doi.org/10.1016/S0031-9384(97)00146-7 Get rights and content

Abstract

McElhinny, T. L., L. Smale and K. E. Holekamp. Patterns of body temperature, activity, and reproductive behavior in a tropical murid rodent, Arvicanthis niloticus. Physiol Behav 62(1) 91–96, 1997.—Nile grass rats (Arvicanthis niloticus), are murid rodents from tropical Africa that exhibit diurnal patterns of wheel-running. In the present paper we describe the temporal organization of several other behaviors in these animals, as well as daily rhythms in their body temperature. In the first experiment, we characterized rhythms of gross motor activity and core body temperature in four adult females implanted with telemetry transmitters and kept on a 12:12 light:dark (LD) cycle. In all animals body temperature and gross motor activity were clearly diurnal, with peaks often occurring around dawn and dusk. In the second experiment we recorded the times of mating and parturition in eight mating couples housed in a 12:12 LD cycle. We monitored animals 24 h a day using a time-lapse video recording system, beginning when males and females were paired, and ending after the birth of the second litter and the associated post-partum copulation. Mating almost always began just before the lights came on, and parturition generally occurred in an “anticrepuscular” pattern, outside of the periods around dawn and dusk. Thus, these animals exhibit an interesting mosaic of temporal adaptations, with some crepuscular tendencies expressed within a predominantly diurnal pattern.

Section snippets

Study Animals

The original stock of 29 individuals from which all study animals were derived was trapped in July and August of 1993, from two locations within the Masai Mara National Reserve in southwestern Kenya. Study animals were all maintained in plastic cages (38 × 34 × 16 cm) with chipped aspen litter, in rooms kept at 23°C, on a 12:12 light:dark (LD) cycle. Animals were provided tap water and Harlan 8640 Teklad 22/5 rodent chow ad lib, and supplemented with carrots and whole oats once a week. Litters

Experiment 1: Activity and Temperature Rhythms

Daily patterns of gross motor activity and body temperature of A. niloticus were highly predictable and precise (Fig. 1). All individuals exhibited some activity at all phases of the LD cycle and had higher average hourly levels of activity during the light phase than during the dark phase (Fig. 2). On average, activity onset (the 20 min interval after the lowest point preceding a steady rise to the morning peak) occurred 2.05 ± 0.33 h before lights-on. All animals exhibited two peaks of

Discussion

Wheel-running rhythms in A. niloticus were previously shown to be diurnal with peaks around dawn and dusk ([21]). In the experiments reported here we have extended these earlier findings by revealing that A. niloticus exhibit a coordinated suite of adaptations to this general pattern of rhythmicity. Specifically, patterns of general activity and body temperature were diurnal, and matings were concentrated in the active period just before the lights came on. Parturition, by contrast, exhibited

Acknowledgements

We are grateful to the Kenya Wildlife Service for permission to export the original wild-caught A. niloticus. We are also grateful to Jacob Pegg and David Kent for their help on this project. The research described in this paper was supported by fellowships to KEH from the David and Lucille Packard Foundation and the Searle Scholars Program/Chicago Community Trust, and by NIMH grant #RO1 MH53433-01.

References (53)

M.J. Bosc
Photoperiodic regulation of the time of birth in rats: Involvement of circadian endogenous mechanisms
Phys. Behav.
(1990)
G.A. Eskes
Neural control of the daily rhythm of sexual behavior in the male golden hamster
Brain Res.
(1984)
A.N. Gilbert et al.
Timing of parturition and postpartum mating in norway rats: Interaction of an interval timer and a circadian gate
Phys. Behav.
(1985)
C.I. Katona et al.
Wheel running rhythms in Arvicanthis niloticus
Phys. Behav.
(1997)
S.M. Reppert et al.
The circadian-gated timing of birth in rats: Disruption by maternal SCN lesions or by removal of the fetal brain
Brain Res.
(1987)
D.L. Rowland et al.
Effect of constant light on parturition and postpartum reproduction in the rat
Phys. Behav.
(1995)
H. Abe et al.
Circadian modulation in photic induction of fos-like immunoreactivity in the suprachiasmatic nucleus cells of the diurnal chipmunk, Eutamias asiaticus
J. Comp. Physiol. A.
(1995)
W.F.H. Ansell
Mammals of northern Rhodesia
(1960)
J. Aschoff
Circadian activity patterns with two peaks
Ecology.
(1970)
F.A. Beach et al.
Diurnal variations in the mating behavior of male rats
Proc. Soc. Exp. Biol. Med.
(1949)

R.J. Blandau et al.

Post-parturitional heat and the time of ovulation in the albino rat. Data on parturition

Anat. Rec.

(1941)

E. Capanna et al.

A cytotaxonomic approach to the systematics of Arvicanthis niloticus (Desmarest, 1822) (Mammalia, Rodentia)

Trop. Zool.

(1988)

M.D. Carleton et al.

Muroid rodents

J.R. Connor et al.

Postpartum estrus in Norway rats

I. Behavior. Biol. Rep.

(1980)

M.J. Delany et al.

Observations of the ecology of rodents from a small arable plot near Kampala, Uganda

Rev. Zol. Bot. Afr.

(1970)

J.-M. Duplantier et al.

Rhythms d'activité chez six espèces de Muridés du Sénégal appartenant aux genres Mastomys, Arvicanthis, Myomys et Dasymys

Mammalia.

(1990)

H.H. Feder

Estrous Cyclicity in Mammals

L.I. Ghobrail et al.

Seasonal variation in the breeding of the Nile rat (Arvicanthis niloticus)

Mammalia.

(1982)

D.F. Hardy

Sexual behavior in continuously cycling rats

Behaviour.

(1972)

R.E. Harlan et al.

Sexual performance as a function of time of day in male and female rats

Biol. Reprod.

(1980)

J.H. Honacki et al.

Mammalian Species of the World: A Taxonomic and Geographic Reference

(1982)

A. Jolly

Primate birth hour

Int. Zoo Yb.

(1973)

D.L. Harrison

The Mammals of Arabia, VIII

(1972)

R.E. Keuhn et al.

Quantitative measurement of sexual receptivity in female rats

Behaviour.

(1963)

J. Kingdon

East African Mammals

Vol. 2B: Hares and Rodents

(1974)

D.C. Klein et al.

Suprachiasmatic Nucleus: The Mind's Clock

(1991)

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Patterns of Body Temperature, Activity, and Reproductive Behavior in a Tropical Murid Rodent, Arvicanthis niloticus

Abstract

Section snippets

Study Animals

Experiment 1: Activity and Temperature Rhythms

Discussion

Acknowledgements

Phys. Behav.

Brain Res.

Phys. Behav.

Phys. Behav.

Brain Res.

Phys. Behav.

Circadian modulation in photic induction of fos-like immunoreactivity in the suprachiasmatic nucleus cells of the diurnal chipmunk, Eutamias asiaticus

J. Comp. Physiol. A.

Mammals of northern Rhodesia

Circadian activity patterns with two peaks

Ecology.

Diurnal variations in the mating behavior of male rats

Proc. Soc. Exp. Biol. Med.

Post-parturitional heat and the time of ovulation in the albino rat. Data on parturition

Anat. Rec.

A cytotaxonomic approach to the systematics of Arvicanthis niloticus (Desmarest, 1822) (Mammalia, Rodentia)

Trop. Zool.

Muroid rodents

Postpartum estrus in Norway rats

I. Behavior. Biol. Rep.

Observations of the ecology of rodents from a small arable plot near Kampala, Uganda

Rev. Zol. Bot. Afr.

Rhythms d'activité chez six espèces de Muridés du Sénégal appartenant aux genres Mastomys, Arvicanthis, Myomys et Dasymys

Mammalia.

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Seasonal variation in the breeding of the Nile rat (Arvicanthis niloticus)

Mammalia.

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Behaviour.

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Biol. Reprod.

Mammalian Species of the World: A Taxonomic and Geographic Reference

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Int. Zoo Yb.

The Mammals of Arabia, VIII

Quantitative measurement of sexual receptivity in female rats

Behaviour.

East African Mammals

Vol. 2B: Hares and Rodents

Suprachiasmatic Nucleus: The Mind's Clock