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Thermoregulatory behaviour of outdoor and commensal populations of mice (Mus musculus domesticus and Mus spretus) in response to cold
Pergamon
03(ffv4565(94)E0005-3
J. therm. Biol. Vol. 19, No. 3, pp. 213-217, 1994 Copyright © 1994ElsevierScienceLtd Printed in Great Britain. All rights reserved
0306-4565/94$7.00+ 0.00
THERMOREGULATORY BEHAVIOUR OF OUTDOOR AND COMMENSAL POPULATIONS OF MICE (MUS MUSCULUS DOMESTICUS AND MUS SPRETUS) IN RESPONSE TO COLD ODILE POULIQUEN-YOUNG Laboratoire d'Eco-Ethologie, Institut des Sciences de l'Evolution, Universit6 des Scienceset Techniques du Languedoc, Place Eug6ne Bataillon, 34060 Montpellier Cedex, France (Received 13 November 1993; accepted in revised form 31 January 1994)
Abstract--1. The behavioural thermoregulatory response to cold exposure in the laboratory was investigated in one commensal and two outdoor populations of the house mouse, Mus musculus domesticus, and in the Western Mediterranean mouse, Mus spretus. 2. The increase in food consumption in the cold showed M. spretus and commensal house mice to be less adapted to cold than outdoor mice, in concordance with their ecological and geographical distributions. 3. Nest building behaviour showed a high inter-individual variation and nests were small even in the cold. Differences in nest weight between populations were not related to natural habitats nor to food consumption. Key Word Index: Mus musculus domesticus; Mus spretus; thermoregulation; food consumption; nest
building; commensalism
INTRODUCTION
For small rodents such as the house mouse, cold adaptation involves several behavioural and physiological traits (e.g. Jakobson, 1981; Barnett and Dickson, 1989). While an increase in body size may occur in response to cold in the laboratory (Barnett and Dickson, 1989), this may not occur in natural habitats (Berry et al., 1978). The amount of brown adipose tissue has been shown to have a low heritability (Lynch and Sulzbach, 1984), which indicates that this physiological trait does not respond to selection any more (Lynch, 1986), although it is a quite important element in individual acclimation. The pelage has been reported to thicken in mice reared in cold temperatures (Al-Hilli and Wright, 1988). Hoarding and torpor have been reported to occur in the house mouse (Hudson and Scott, 1979; Morton, 1978; Barnett et al., 1984). Nesting behaviour in response to low temperatures, however, has been the response to cold most studied in this species. Coldacclimated animals tend to build heavier nests than do warm-acclimated animals. Nest building can also Current address: Institute for Science and Technology Policy, Murdoch University, Murdoch WA 6150, Australia.
be subject to artificial selection in laboratory strains of mice, indicating a genetic basis for this behaviour (Lynch and Hegmann, 1972; Lynch, 1986). In Peromyscus and the house mouse, nest building differentiation between natural populations has also been correlated with their geographical origins (King et al., 1964; Layne, 1969; Plomin and Manosevitz, 1974; Glaser and Lustick, 1975; Lynch, 1986), which indicates that building bigger nests is advantageous in cold environments. In the genus Mus, only M . musculus Linn6 (comprising M . m. domesticus Rutty) is commensal with man (Sage, 1981). Human-made habitats such as buildings and haystacks provide shelter and a stable food supply and enable the species to inhabit all of Europe. Along the Mediterranean coast, however, some populations of M. m. domesticus are independent of human activities. They are thus less protected against climatic conditions and experience greater fluctuations in their food supply. They are referred to below as outdoor populations. In some areas, these are sympatric and compete with M. spretus Lataste, the distribution of which is confined to the Western Mediterranean. In the south of France, M. spretus is not considered to be commensal as it is not found in buildings (Orsini et al., 1982; Cassaing and Croset,
213
214
ODILE POULIQUEN-YOUNG
1985). The study was designed to test the hypothesis that, although being of similar shape and weight, individuals from these three populations should differ in their level of cold adaptation, according to their ecological origin. Commensal mice should be able to sustain high energy requirements being more or less sheltered from the environmental conditions while, in comparison, outdoor house mice nesting behaviour should be well developed and the food requirements of these animals should be low since they will have become adapted to the lower ambient temperatures and the lower availability of food experienced in winter. Accordingly, M. spretus should present a low level of cold adaptation given its Mediterranean distribution. MATERIALS AND METHODS
Origin o f animals
Two outdoor populations of M. m. domesticus from the Mediterranean region were sampled, one from Ostricconi in North-Western Corsica (Corsica), and the other from near Montpellier in Southern France (S. France). M. spretus also came from around Montpellier. The demography and spatial structure of these populations have been described elsewhere (Orsini et al., 1982; Cassaing and Croset, 1985; Granjon and Cheylan, 1988). The commensal house mice were trapped inside buildings in the Po valley in Northern Italy (N. Italy). The chromosomal numbers of house mice in this region are different from those of house mice elsewhere, having fixed Robertsonian translocations (Gropp et al., 1982). In the area where the animals were trapped, mice belong to the Milano II chromosomal race with a karyotype of 2n = 24 (Gropp et al., 1982). These populations are usually found indoors and are only found outdoors during the warmest season (Auffray et al., 1990). The temperature of the coldest month averages 0°C in Northern Italy, 5°C in Montpellier and 9°C in North Corsica. Experimental procedure
Mice were housed in pairs under a natural photoperiod at 22-24°C. Offspring were weaned at 1 month, housed in pairs with food, water and cotton wool ad libitum. They were used for the experiment when over 3 months old. The females were neither pregnant nor lactating. A total of 69 individuals were tested: 14 M. spretus (5 males, 9 females) and 55 M. m. domesticus (33 males and 22 females): 11 from Corsica, 22 N. Italy and 22 S. France. The nesting behaviour methodology followed the experimental procedure of Lynch (1986). Individual animals were put in cages at room temperature
(22-24°C). On each day, for 4 days, they were provided with 10 g hydrophobic cotton wool placed on top of the wire lid. The nest built was removed daily and the remaining cotton weighed. The nesting score is the total weight of cotton used during the 4 days. Four to 5 food pellets (12,000 J/kg) were placed on the litter and weighed each day. Food was replenished as necessary. The body weight was recorded at the beginning and end of the experiment and the mean used to calculate food consumption (g food consumed daily/g body wt). Next, the mice were put in a cold room (3-7°C) for 10 days. The experimental procedure was then repeated in the cold room for four days. A previous experiment had revealed no change of the nesting score and of the food consumption variables with a longer period in the cold. The stability of the food consumption and nesting score variables during the four days of each experiment was confirmed by a Friedman analysis of variance for each individual (Siegel and Castellan, 1988). RESULTS
M. m. domestieus
There was no significant differences between males and females in nesting score, body weight or food consumption across populations. The data of both sexes were therefore pooled. At both temperatures, there were no significant differences in body weights between the three samples (Table 1). There was no significant body weight increase in the interval between the two temperature experiments for each sample (Corsica: Wilcoxon T = 30, n = 10; S. France: T = 74.5, n = 21; N. Italy: T = 50, n = 19; P > 0.05 for each sample). At 22-24°C, the three samples did not differ in food consumption, averaging 0.18 g food/g body weight/ day (Table 1). When the animals were placed under the cold temperature, food consumption increased in all individuals (Wilcoxon T = 0, P < 0.01 for each sample). The commensal mice consumed significantly more food in relation to their body weight than the outdoor mice. The latter populations did not differ from one another (Table 1). At 22-24°C, mice from S. France built smaller nests than the mice from the other samples. At 5°C, the differences between the samples were no longer statistically significant (Table 1). There was however a very high inter-individual variation at both temperatures and the distribution of nesting scores remained skewed towards low values even under the cold temperature. At 22-24°C, 60% of the mice had a nesting score equal to or less than 8 g. While 76% of the mice increased their nesting score when placed
Thermoregulatory behaviour of outdoor and commensal populations of mice
215
Table 1. Means ( + SD) of body weight (g), daily food consumption (g food/g body weight) and nesting score (g) of M. m. domesticus from three origins, at two temperatures (Warm: 22-24°C, Cold: 3-7°C) Origin of populations Number of animals Warm Cold Body weight Warm Cold Food consumption Warm Cold Nesting score Warm Cold
Corsica
S. France
N. Italy
11 10
22 21
22 19
16.4 ___3.0a 17.1 __+2.8 a
15.3 +__1.7~ 15.6 __+1.6a
15.5 + 3.0a 16.1 __+3.P
0.17 ___0.04 ~ 0.29 ___0.06 a'b
0.20 ___0.05 a 0.31 __+0.05~'b'
0.18 ___0.04a 0.36 __+0.08 b'b'
8.9 ___7.1 a'b 17.2 +__14.0a
3.8 ___3.7 b'c 7.3 __+5.3~
9.4 + 6.8 a'c 11.0 _+ 8.6~
Statistical differences between population: ~P > 0.05; b,b'p < 0.05; cP < 0.01 (Body Weight and Food Consumption: Student's t-test; Nesting Score: Mann-Whitney).
in the cold temperature, this increase was slight for m o s t o f them: 4 8 % of the animals still presented a nesting score of 8 g or less. Only 9 mice h a d a nesting score o f more t h a n 16 g u n d e r cold temperature. T h e r e were n o significant correlations between food c o n s u m p t i o n , nesting score a n d b o d y weight at 22-24°C. In the cold, the heaviest mice ate less relative to their b o d y weight ( S p e a r m a n r = - 0 . 6 0 , P < 0.01, n = 50). Low food c o n s u m p t i o n was correlated with heavier nests (r = - 0 . 4 4 , P < 0.01), b u t the correlation between body weight a n d nesting score was not significant (r = 0.25, P > 0.05). M . spretus
The body weight of the animals did n o t change between the two temperatures. The food c o n s u m p tion was m u c h higher after cold acclimation, but the nesting score r e m a i n e d low (Table 2). There was n o correlation between food c o n s u m p t i o n , body weight a n d nesting score at either temperature. M . spretus were significantly lighter t h a n M . m. domesticus at b o t h temperatures. Their food c o n s u m p t i o n at w a r m temperature, however, was equivalent to t h a t o f M. m. domesticus samples. In the cold it equalled t h a t of the c o m m e n s a l house mice ( t = 0 . 3 8 , df=21, P > 0.05). T h e nesting score was low a n d n o t different from t h a t o f the S. F r a n c e house mice in the w a r m ( M a n n - W h i t n e y z = 0.94, P > 0.05), but it was the
lowest o f the four m o u s e samples in the cold ( P < 0.01 for each comparison).
DISCUSSION
All individuals responded to a reduction in temperature by increasing their food intake. F o r some individuals, the daily food intake reached up to 4 5 % o f their b o d y weight. M. spretus a n d c o m m e n s a l M. m. domesticus ate m o r e in relation to their body weight t h a n the o u t d o o r M . m. domesticus. These results are consistent with the basal m e t a b o l i s m in cold t e m p e r a t u r e m e a s u r e d o n the same p o p u l a t i o n s (Auffray a n d Navajas, personal c o m m u n i c a t i o n ) . Thus, high energy requirements can explain the strictly M e d i t e r r a n e a n distribution of M. spretus (Orsini et al., 1982) a n d the c o m m e n s a l i s m o f house mice in N o r t h e r n Italy, region subjected to a continental climate with very cold winters (Auffray a n d Vanlerberghe, 1989). In contrast, o u t d o o r M. rn. domesticus present a lower metabolism t h a n the c o m m e n s a l p o p u l a t i o n a n d M . spretus after cold acclimation (Auffray a n d Navajas, personal communication). This accords with the lower food cons u m p t i o n recorded in this study. The energy requirements o f the South-Western E u r o p e a n mouse p o p u l a t i o n s after cold acclimation are therefore con-
Table 2. Means ( + SD) of body weight (g), daily food consumption (g food/g body weight) and nesting score (g) in M. spretus (n = 14) at two temperatures (Warm: 22-24°C; Cold: 3-7°C)
Warm temperature Cold temperature
Body weight
Food consumption
Nesting score
13.2 + 1.8a 13.0 + 1.2a
0.20 + 0.06c 0.37 __+0.07 c
2.3 + 2.5a 2.9 ___3.0a
Difference between Cold and Warm experiment (Wilcoxon) ap > 0.05; cP < 0.01.
216
ODILE POULIQUEN-YOUNG
sistent with their ecological and geographical distributions. The data on nest building behaviour did not, however, conform to these results. According to different studies on natural populations (e.g. Glaser and Lustick, 1975; Lynch, 1986), one would have expected to find that the outdoor house mice were building bigger nests than their commensal counterparts because of their continual exposure to the climate, and to M. spretus because of the strict Mediterranean distribution of this species. Bigger nests would also have been expected after cold acclimation, and again outdoor house mice should have done better in this respect than the other two mouse poulations. The data were not consistent with these hypotheses, in a great part because the nesting score variable presented such a high inter-individual variation. Its coefficient of variation was above 70%, while it did not exceed 30% for the food consumption variable. This individual variation in nest building has also been found in Peromyscus (King et al., 1964; Layne, 1969) and in commensal populations of the house mice (Plomin and Manosevitz, 1974; Lynch, 1986). After exposure to cold, there was no increase of the nest weight for most individuals and most nests remained small. Any interpretation of population differences in nest building behaviour is therefore difficult. For example, M. spretus presented very low nesting scores and no increase between the two environmental temperatures, which could indicate poor adaptation to cold. When compared with other studies, the findings on M . m. domesticus, however, cast a doubt on this simple interpretation. U n d e r a similar methodology, Lynch (1986) recorded an increase in nest weight in the cold of more than 400% in her study of North American populations of commensal house mice, while her data on food consumption are similar to those of the present study. Barnett and Hocking (1981) and Barnett et al. (1984) give evidence that nesting behaviour could meet needs other than thermoregulation. A decline in nest building when more space or alternative activities were available led these authors to conclude that nest building may compete with exploratory behaviour and that the material provided could be valued for hoarding rather than for insulation. If nest building behaviour is in competition with exploration or hoarding, the high inter-individual variation found in this study may indicate individual variation in these two non-thermoregulatory behaviours rather than in nest building per se. In the present study, food consumption was a good indicator and nest building a poor indicator of adaptation to cold of both M. spretus and M. m. domesticus. This concurs with the suggestion by Barnett and
Dickson (1989) that the house mouse (and its relatives) do not present a single cold adaptation pattern. Furthermore, individual nesting behaviour may not reflect what happens in natura where the social act of huddling is common. It can act as a buffer between the individual and the environment and attenuates the need for individual adaptation to environmental conditions. Acknowledgements--I would like to thank J.-C. Auffray, S. Barker, S. A. Barnett, R. Dickson, G. Singleton and G. E. Young who kindly commented on earlier drafts of this manuscript. REFERENCES
AI-Hilli F. and Wright E. A. (1988) The effects of environmental temperature on the growth of hair in the mouse. J. therm. Biol. 13, 21-24. Auffray J.-C. and Vanlerberghe F. (1989) Commensalism in relation to man: involuntary impact of man on the evolution of the house mouse (Mus musculus). Vth International Conference on the relationship between humans and animals. Monaco, 1989. Auffray J.-C., Belkhir K., Cassaing J., Britton-Davidian J. and Croset H. (1990) Outdoor occurrence in Robertsonian and standard populations of the House mouse. Vie et Milieu 40, 111-118. Barnett S. A. and Dickson R. G. (1989) Wild mice in the cold: some findings on adaptation. Biol. Rev. 64, 317-340. Barnett S. A. and Hocking W. E. (198t) Are nests built for fun? Effects of alternative activities on nest-building by wild house mice. Behav. Neur. Biol. 31, 73-81. Barnett S. A., Bammer G. and Mackay C. E. (1984) Nest building or hoarding? Effects of novelty and environmental temperature on the behaviour of wild house mice, with a brief review. Exp. Anita. Behav. 3, 1-8. Berry R. J., Peters J. and Van Aarde R. J. (1978) Subantarctic house mice: colonization, survival and selection. J. Zool. Lond. 184, 127-141. Cassaing J. and Croset H. (1985) Organisation spatiale, comprtition et dynamique des populations sauvages de souris (Mus spretus Lataste et Mus musculus domesticus Rutty) du Midi de la France, Z. Siiugetierkunde 50, 271-284. Glaser R. H. and Lustick S. (1975) Energetics and nesting behavior of the northern white-footed mouse Peromyscus leucopus noveboracensis. Physiol. Zool. 48, 105-I 13. Granjon L. and Cheylan G. (1988) Mrcanismes de coexistence dans une guilde de Muridrs insulaires (Rattus rattus L., Apodemus sylvaticus L. et Mus musculus domesticus Rutty) en Corse: Consrquences 6volutives. Z. Sdugetierkunde 53, 301-316. Gropp A., Winking H., Redi C., Capanna E., BrittonDavidian J. and Noack G. (1982) Robertsonian karyotype variation in wild house mice from RhaetoLombardia. Cytogenet. Cell. Genet. 34, 67-77. Hudson J. W. and Scott I. M. (1979) Daily torpor in the laboratory mouse Mus musculus, var. albino. Physiol. Zool. 52, 205-218. Jakobson M. E. (1981) Physiological adaptability: the response of the house mouse to variations in the environment. Symp. Zool. Soc., Lond. 47, 301-335.
Thermoregulatory behaviour of outdoor and commensal populations of mice King J. A., Maas D. and Weisman R. G. (1964) Geographic variation in nest size among species of Peromyscus. Evolution 18, 230-234. Layne J. N. (1969) Nest building behavior in three species of deer mice, Peromyscus. Behaviour 35, 288-303. Lynch C. B. (1986) Genetic basis of cold adaptation in laboratory and wild mice, Mus musculus domesticus. In Living in the cold; Physiological and Biochemical Adaptation (Edited by Heller H. C. and Musacchia X. J.)
pp. 497-503. Elsevier, New York. Lynch C. B. and Hegmann J. P. (1972) Genetic differences influencing behavioral temperature regulation in small mammals. I. Nesting by Mus musculus. Behavior Genetics 2, 43-53. Lynch C. B. and Sulzbach D. S. (1984) Quantitative genetic analysis of temperature regulation in Mus musculus. II. Diallel analysis of individual traits. Evolution 38, 527-540.
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Morton S. R. (1978) Torpor and nest sharing in free living Sminthopsis crassicaudata (Marsupalia) and Mus musculus (Rodentia). J. Mammal. 59, 569-575. Orsini P., Cassaing J., Duplantier J.-M. and Croset H, (1982) Premi6res donn6es sur r6cologie des populations naturelles de souris, Mus spretus Lataste et Mus musculus domesticus Rutty, dans le Midi de la France. Rev. Ecol. 36, 321-336. Plomin R. J. and Manosevitz M. (1974) Behavioral polytypism in wild Mus musculus. Behav. Genet. 4, 145-157. Sage R. D. (1981) Wild mice. In The Mouse in Biomedical Research (Edited by Foster H. L., Small J. D. and Fox J. G.), Vol. I, pp. 39-90. Academic Press, San Diego. Siegel S. and Castellan N. J. (1988) Non-Parametric Statistics for the Behavioral Sciences. 2nd edition. McGraw-Hill, New York.
03(ffv4565(94)E0005-3
J. therm. Biol. Vol. 19, No. 3, pp. 213-217, 1994 Copyright © 1994ElsevierScienceLtd Printed in Great Britain. All rights reserved
0306-4565/94$7.00+ 0.00
THERMOREGULATORY BEHAVIOUR OF OUTDOOR AND COMMENSAL POPULATIONS OF MICE (MUS MUSCULUS DOMESTICUS AND MUS SPRETUS) IN RESPONSE TO COLD ODILE POULIQUEN-YOUNG Laboratoire d'Eco-Ethologie, Institut des Sciences de l'Evolution, Universit6 des Scienceset Techniques du Languedoc, Place Eug6ne Bataillon, 34060 Montpellier Cedex, France (Received 13 November 1993; accepted in revised form 31 January 1994)
Abstract--1. The behavioural thermoregulatory response to cold exposure in the laboratory was investigated in one commensal and two outdoor populations of the house mouse, Mus musculus domesticus, and in the Western Mediterranean mouse, Mus spretus. 2. The increase in food consumption in the cold showed M. spretus and commensal house mice to be less adapted to cold than outdoor mice, in concordance with their ecological and geographical distributions. 3. Nest building behaviour showed a high inter-individual variation and nests were small even in the cold. Differences in nest weight between populations were not related to natural habitats nor to food consumption. Key Word Index: Mus musculus domesticus; Mus spretus; thermoregulation; food consumption; nest
building; commensalism
INTRODUCTION
For small rodents such as the house mouse, cold adaptation involves several behavioural and physiological traits (e.g. Jakobson, 1981; Barnett and Dickson, 1989). While an increase in body size may occur in response to cold in the laboratory (Barnett and Dickson, 1989), this may not occur in natural habitats (Berry et al., 1978). The amount of brown adipose tissue has been shown to have a low heritability (Lynch and Sulzbach, 1984), which indicates that this physiological trait does not respond to selection any more (Lynch, 1986), although it is a quite important element in individual acclimation. The pelage has been reported to thicken in mice reared in cold temperatures (Al-Hilli and Wright, 1988). Hoarding and torpor have been reported to occur in the house mouse (Hudson and Scott, 1979; Morton, 1978; Barnett et al., 1984). Nesting behaviour in response to low temperatures, however, has been the response to cold most studied in this species. Coldacclimated animals tend to build heavier nests than do warm-acclimated animals. Nest building can also Current address: Institute for Science and Technology Policy, Murdoch University, Murdoch WA 6150, Australia.
be subject to artificial selection in laboratory strains of mice, indicating a genetic basis for this behaviour (Lynch and Hegmann, 1972; Lynch, 1986). In Peromyscus and the house mouse, nest building differentiation between natural populations has also been correlated with their geographical origins (King et al., 1964; Layne, 1969; Plomin and Manosevitz, 1974; Glaser and Lustick, 1975; Lynch, 1986), which indicates that building bigger nests is advantageous in cold environments. In the genus Mus, only M . musculus Linn6 (comprising M . m. domesticus Rutty) is commensal with man (Sage, 1981). Human-made habitats such as buildings and haystacks provide shelter and a stable food supply and enable the species to inhabit all of Europe. Along the Mediterranean coast, however, some populations of M. m. domesticus are independent of human activities. They are thus less protected against climatic conditions and experience greater fluctuations in their food supply. They are referred to below as outdoor populations. In some areas, these are sympatric and compete with M. spretus Lataste, the distribution of which is confined to the Western Mediterranean. In the south of France, M. spretus is not considered to be commensal as it is not found in buildings (Orsini et al., 1982; Cassaing and Croset,
213
214
ODILE POULIQUEN-YOUNG
1985). The study was designed to test the hypothesis that, although being of similar shape and weight, individuals from these three populations should differ in their level of cold adaptation, according to their ecological origin. Commensal mice should be able to sustain high energy requirements being more or less sheltered from the environmental conditions while, in comparison, outdoor house mice nesting behaviour should be well developed and the food requirements of these animals should be low since they will have become adapted to the lower ambient temperatures and the lower availability of food experienced in winter. Accordingly, M. spretus should present a low level of cold adaptation given its Mediterranean distribution. MATERIALS AND METHODS
Origin o f animals
Two outdoor populations of M. m. domesticus from the Mediterranean region were sampled, one from Ostricconi in North-Western Corsica (Corsica), and the other from near Montpellier in Southern France (S. France). M. spretus also came from around Montpellier. The demography and spatial structure of these populations have been described elsewhere (Orsini et al., 1982; Cassaing and Croset, 1985; Granjon and Cheylan, 1988). The commensal house mice were trapped inside buildings in the Po valley in Northern Italy (N. Italy). The chromosomal numbers of house mice in this region are different from those of house mice elsewhere, having fixed Robertsonian translocations (Gropp et al., 1982). In the area where the animals were trapped, mice belong to the Milano II chromosomal race with a karyotype of 2n = 24 (Gropp et al., 1982). These populations are usually found indoors and are only found outdoors during the warmest season (Auffray et al., 1990). The temperature of the coldest month averages 0°C in Northern Italy, 5°C in Montpellier and 9°C in North Corsica. Experimental procedure
Mice were housed in pairs under a natural photoperiod at 22-24°C. Offspring were weaned at 1 month, housed in pairs with food, water and cotton wool ad libitum. They were used for the experiment when over 3 months old. The females were neither pregnant nor lactating. A total of 69 individuals were tested: 14 M. spretus (5 males, 9 females) and 55 M. m. domesticus (33 males and 22 females): 11 from Corsica, 22 N. Italy and 22 S. France. The nesting behaviour methodology followed the experimental procedure of Lynch (1986). Individual animals were put in cages at room temperature
(22-24°C). On each day, for 4 days, they were provided with 10 g hydrophobic cotton wool placed on top of the wire lid. The nest built was removed daily and the remaining cotton weighed. The nesting score is the total weight of cotton used during the 4 days. Four to 5 food pellets (12,000 J/kg) were placed on the litter and weighed each day. Food was replenished as necessary. The body weight was recorded at the beginning and end of the experiment and the mean used to calculate food consumption (g food consumed daily/g body wt). Next, the mice were put in a cold room (3-7°C) for 10 days. The experimental procedure was then repeated in the cold room for four days. A previous experiment had revealed no change of the nesting score and of the food consumption variables with a longer period in the cold. The stability of the food consumption and nesting score variables during the four days of each experiment was confirmed by a Friedman analysis of variance for each individual (Siegel and Castellan, 1988). RESULTS
M. m. domestieus
There was no significant differences between males and females in nesting score, body weight or food consumption across populations. The data of both sexes were therefore pooled. At both temperatures, there were no significant differences in body weights between the three samples (Table 1). There was no significant body weight increase in the interval between the two temperature experiments for each sample (Corsica: Wilcoxon T = 30, n = 10; S. France: T = 74.5, n = 21; N. Italy: T = 50, n = 19; P > 0.05 for each sample). At 22-24°C, the three samples did not differ in food consumption, averaging 0.18 g food/g body weight/ day (Table 1). When the animals were placed under the cold temperature, food consumption increased in all individuals (Wilcoxon T = 0, P < 0.01 for each sample). The commensal mice consumed significantly more food in relation to their body weight than the outdoor mice. The latter populations did not differ from one another (Table 1). At 22-24°C, mice from S. France built smaller nests than the mice from the other samples. At 5°C, the differences between the samples were no longer statistically significant (Table 1). There was however a very high inter-individual variation at both temperatures and the distribution of nesting scores remained skewed towards low values even under the cold temperature. At 22-24°C, 60% of the mice had a nesting score equal to or less than 8 g. While 76% of the mice increased their nesting score when placed
Thermoregulatory behaviour of outdoor and commensal populations of mice
215
Table 1. Means ( + SD) of body weight (g), daily food consumption (g food/g body weight) and nesting score (g) of M. m. domesticus from three origins, at two temperatures (Warm: 22-24°C, Cold: 3-7°C) Origin of populations Number of animals Warm Cold Body weight Warm Cold Food consumption Warm Cold Nesting score Warm Cold
Corsica
S. France
N. Italy
11 10
22 21
22 19
16.4 ___3.0a 17.1 __+2.8 a
15.3 +__1.7~ 15.6 __+1.6a
15.5 + 3.0a 16.1 __+3.P
0.17 ___0.04 ~ 0.29 ___0.06 a'b
0.20 ___0.05 a 0.31 __+0.05~'b'
0.18 ___0.04a 0.36 __+0.08 b'b'
8.9 ___7.1 a'b 17.2 +__14.0a
3.8 ___3.7 b'c 7.3 __+5.3~
9.4 + 6.8 a'c 11.0 _+ 8.6~
Statistical differences between population: ~P > 0.05; b,b'p < 0.05; cP < 0.01 (Body Weight and Food Consumption: Student's t-test; Nesting Score: Mann-Whitney).
in the cold temperature, this increase was slight for m o s t o f them: 4 8 % of the animals still presented a nesting score of 8 g or less. Only 9 mice h a d a nesting score o f more t h a n 16 g u n d e r cold temperature. T h e r e were n o significant correlations between food c o n s u m p t i o n , nesting score a n d b o d y weight at 22-24°C. In the cold, the heaviest mice ate less relative to their b o d y weight ( S p e a r m a n r = - 0 . 6 0 , P < 0.01, n = 50). Low food c o n s u m p t i o n was correlated with heavier nests (r = - 0 . 4 4 , P < 0.01), b u t the correlation between body weight a n d nesting score was not significant (r = 0.25, P > 0.05). M . spretus
The body weight of the animals did n o t change between the two temperatures. The food c o n s u m p tion was m u c h higher after cold acclimation, but the nesting score r e m a i n e d low (Table 2). There was n o correlation between food c o n s u m p t i o n , body weight a n d nesting score at either temperature. M . spretus were significantly lighter t h a n M . m. domesticus at b o t h temperatures. Their food c o n s u m p t i o n at w a r m temperature, however, was equivalent to t h a t o f M. m. domesticus samples. In the cold it equalled t h a t of the c o m m e n s a l house mice ( t = 0 . 3 8 , df=21, P > 0.05). T h e nesting score was low a n d n o t different from t h a t o f the S. F r a n c e house mice in the w a r m ( M a n n - W h i t n e y z = 0.94, P > 0.05), but it was the
lowest o f the four m o u s e samples in the cold ( P < 0.01 for each comparison).
DISCUSSION
All individuals responded to a reduction in temperature by increasing their food intake. F o r some individuals, the daily food intake reached up to 4 5 % o f their b o d y weight. M. spretus a n d c o m m e n s a l M. m. domesticus ate m o r e in relation to their body weight t h a n the o u t d o o r M . m. domesticus. These results are consistent with the basal m e t a b o l i s m in cold t e m p e r a t u r e m e a s u r e d o n the same p o p u l a t i o n s (Auffray a n d Navajas, personal c o m m u n i c a t i o n ) . Thus, high energy requirements can explain the strictly M e d i t e r r a n e a n distribution of M. spretus (Orsini et al., 1982) a n d the c o m m e n s a l i s m o f house mice in N o r t h e r n Italy, region subjected to a continental climate with very cold winters (Auffray a n d Vanlerberghe, 1989). In contrast, o u t d o o r M. rn. domesticus present a lower metabolism t h a n the c o m m e n s a l p o p u l a t i o n a n d M . spretus after cold acclimation (Auffray a n d Navajas, personal communication). This accords with the lower food cons u m p t i o n recorded in this study. The energy requirements o f the South-Western E u r o p e a n mouse p o p u l a t i o n s after cold acclimation are therefore con-
Table 2. Means ( + SD) of body weight (g), daily food consumption (g food/g body weight) and nesting score (g) in M. spretus (n = 14) at two temperatures (Warm: 22-24°C; Cold: 3-7°C)
Warm temperature Cold temperature
Body weight
Food consumption
Nesting score
13.2 + 1.8a 13.0 + 1.2a
0.20 + 0.06c 0.37 __+0.07 c
2.3 + 2.5a 2.9 ___3.0a
Difference between Cold and Warm experiment (Wilcoxon) ap > 0.05; cP < 0.01.
216
ODILE POULIQUEN-YOUNG
sistent with their ecological and geographical distributions. The data on nest building behaviour did not, however, conform to these results. According to different studies on natural populations (e.g. Glaser and Lustick, 1975; Lynch, 1986), one would have expected to find that the outdoor house mice were building bigger nests than their commensal counterparts because of their continual exposure to the climate, and to M. spretus because of the strict Mediterranean distribution of this species. Bigger nests would also have been expected after cold acclimation, and again outdoor house mice should have done better in this respect than the other two mouse poulations. The data were not consistent with these hypotheses, in a great part because the nesting score variable presented such a high inter-individual variation. Its coefficient of variation was above 70%, while it did not exceed 30% for the food consumption variable. This individual variation in nest building has also been found in Peromyscus (King et al., 1964; Layne, 1969) and in commensal populations of the house mice (Plomin and Manosevitz, 1974; Lynch, 1986). After exposure to cold, there was no increase of the nest weight for most individuals and most nests remained small. Any interpretation of population differences in nest building behaviour is therefore difficult. For example, M. spretus presented very low nesting scores and no increase between the two environmental temperatures, which could indicate poor adaptation to cold. When compared with other studies, the findings on M . m. domesticus, however, cast a doubt on this simple interpretation. U n d e r a similar methodology, Lynch (1986) recorded an increase in nest weight in the cold of more than 400% in her study of North American populations of commensal house mice, while her data on food consumption are similar to those of the present study. Barnett and Hocking (1981) and Barnett et al. (1984) give evidence that nesting behaviour could meet needs other than thermoregulation. A decline in nest building when more space or alternative activities were available led these authors to conclude that nest building may compete with exploratory behaviour and that the material provided could be valued for hoarding rather than for insulation. If nest building behaviour is in competition with exploration or hoarding, the high inter-individual variation found in this study may indicate individual variation in these two non-thermoregulatory behaviours rather than in nest building per se. In the present study, food consumption was a good indicator and nest building a poor indicator of adaptation to cold of both M. spretus and M. m. domesticus. This concurs with the suggestion by Barnett and
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