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Social facilitation of reduced oxygen consumption in Mus musculus and Meriones unguiculatus
SOCIAL FACILITATION OF REDUCED OXYGEN CONSUMPTION IN MUS MUSCULUS ~~R~O~~S ~~~U~C~~~~US RORI:RT A. MARTIN‘. MARIO FIORCNTINI, and FREDERICK Department
of Biological
and Allied Health Sciences. Fairleigh Madison. New Jersey 07940. U.S.A.
AND
CONNORS
Dickinson
University.
The short-term resting rates of oxygen consumption of laboratory white mice (Mus IV~~.Sctrfns) and Mongolian gerbils (Meriones ur~yuicu/aru.s) were measured by closed system manometry. 2. Metabolic rates of animals tested illdividua~ly were compared to those of huddled trios and trios in which the animals were tested simultaneously but prevented from physical contact (separated trios) at tcmpcratures ranging from 9 25 C. 3. Rates of increase of weight-specific resting metabolism were greatest for animals tested individually. 4. There was no significant difference in the rates of increase of oxygen consumption between huddled and separated trios in either species. Abstract--.I.
phenomena of interest to the senior author. They are not completely comparable, but the results lead us to seriously question an accepted theoretical mechanism of mammalian energetics. For this reason we fee1 that the results should be reported now. Further. we hope that this paper will spur additional investigations into the physiological basis of sociality (sociophysiology).
Il\iTRODL:CTION Aggregation small
is a behavioral
pattern
common
to many
mammals.
Often referred to as h~iddling, it is especially apparent at low ambient temperatures. The metabolic consequences of this behavior have been studied in Apoder~us u~~rc~riu.s(Gorecki, 1968 ; Terti!, 1972). ~~~~~~~~~~~~.s .~~~~j~~~~~s (Fedyk, 197 I), ~~if~ro~ontori1~3 IN~~~~&~Ls (Pearson, 19hO), F~ro~~~yxw lrucopus (Sealander, 1952; Mark, !974), Meriotles urlgtticularus (McManus & Singer, 1975). MUS ~nusculus (Pearson, 1947 ; Prychodko, 1958; Stanier. 1973, C~~~j~~o~o~~s ~l~fr~~~i~s (Gorecki. 1969; Gebczynska & Gebczynski, 1971 ; Gebczynski, 1969). Microtus urvalis (Trojan & Wojciechowska. 196X), Miuotus p~~t~r~s~~lranicus (Wiegert, 1961). and Strs scrqfir (Mount, 1960). At low ambient temperatures aggregates demonst~te significantly lower oxygen or food consumption when compared on a weight-specific basis to animals tested individually. The cost of maintenance of core temperature also tends to decrease (Mount, 1960). The cause of these energetic and thermal benefits has been taken to be a decrease of surface area to mass ratio in aggregates. Although this may be true, another factor may be involved. As social animals. many small mammals appear to be comforted by the presence of others of the same species. This is a conclusion gained from observation of laboratory and wild animals, and is also confirmed in the literature (Wilson. 197.5). If we consider the possibility that a comfort factor is involved, then we can postulate that the decrease of energy consumption and utilization recorded by many authors may be composed of at least two components: one physical, relating to decreased surface area as an aggregate increases in mass; and one psycho-physiological, relating to the immediate presence of conspecific individuals. The purpose of this study is to test this hypothesis by comparing the oxygen consumption of three animals (a trio) under two conditions: in physical contact (huddled), and restrained from physical contact (separated). The experiments reported here are undergraduate projects and represent preliminary investigations of
MATERIALS AND METHODS Twelve laboratory white mice, strain BALBIC. and IX gerbils of both sexes were used in this study. Trios were composed of both sexes chosen at random. The gerbils derive from an initial group of LO pairs obtained from Tumblebrook Farm in 1969. This is the same laboratory population of gerbils (but not the same individuals) tested by McManus & Singer (1975). None of the females were pregnant or lactating. Weight of the white mice averaged 26.5 g, ranging from 18.5 to 34.0 e. Weirht of the gerbils averaged 6i.lg; range 55.0-75.0 g.-White-mice were hvoused individually in plastic containers. and were chosen at random to comprise test trios prior to each test. The gerbils were housed as cagemate trios. Metabolic data for the two species are not, therefore, strictly comparable. Cedar shavings were provided as bedding material. Food (Purina Lab Chow) and water were provided ud lihirtrin. Photoperiod was controlled: I6 hr light and 8 hr dark. Ambient temperature was maintained at 21 + 2’C. Experimental chambers were constructed from 3.8 1. paint cans. Three copper tubes were fashioned as entry ports in each lid. A dial thermometer was inserted in the largest. central tube (7 mm diameter). Another tube (5 mm diameter) allowed for entry of oxygen injected by a 30mI syringe. and the third (5 mm diameter) was connected in series with a manometer block (Carolma Biological Supply Company), A blank chamber (thermobarometer) was connected to the opposite side of the manometer block to complete the closed system. Brody’s Manometer Fluid acted as the volume indicator, and (indicating type) soda lime was used to absorb C02. Animals rested above the soda lime on a wire platform covered by a piece of filter paper. This system is modified from the Zollinhofer Manometer (Dabney & Zoltinhofer. 1968) and has been described elsewhere by McManus & Singer (1975). Double wire mesh separated the experimental chamber into three equal secti&. Physical contact was mandated by the placement of trios in one of the sections. but was impossible when one individual was placed in each section. 519
520
ROIXKI
A. MAKUN.
4
MARIO FIOKI WINI
and FRtUf:KI(.K
CONNOKS
IO
!I
6 t
4-
6 7
1 IO
t
I 20
I 15
!j 30
25
PC) +7 standard errors consumption of individual Mu, ~UUSXY~~UX The mean. _observed range, and number of runs ilre provided for each temperature. To
Oxygen
Ambient tcmpcrature in the cxperimcntal chumber was maintained within iO.5’C by a Magna Whirl Constant Temperature Bath containing a solution of tap wilter and salt. The experimental chamber and thermobarametric chamber were submerged during all tests to control tempcrature fluctuations. Above room temperature. water temperoturc wx maintained strictly by the water bath. Water temperature was lowered below this point by the addition of ice and maintained with il Lab Line Immersion Cooler. All animals were f~lstcd for 5 hr prior to testing. Oxygen consumption of separated and huddled trio white mice was measured at IO. IS, and 20 C. Control single white mice were tested at IO. 15, 20. 25. and 30 C. McManus & Singer (1975) provided data for single and huddled trio gerbils. We tested only separated trios. at ;1 range of temperatures between 9 and 115 C. All test individuals were allowed 30 40min to adjust to the test environment before mcasurcments were made. Testing took place between noon and midmght; generally in the curly evenings. Each oxygen consumption determination lasted between I8 and 24 min. with recordings made at 2-min intervals. Results
wcrc corrected
of the mean.
Singles;
Separated
Huddled
,’ = -0.46.~ + 13.25
(1)
?‘ = -0.27.X + 10.00
(2)
1’ = - 0.33.Y + 10.03
(3)
trios;
trios:
Table 1 presents the mean values for the three test conditions. Both trio groups generally demonstrate lower metabolic rates than individuals, although at 2O’C separated trios had higher average oxygen con-
to STP. RESL’LTS
Figure 1 depicts the temperature dependent metabolic pattern of A4us r~~usculus tested individually. Computed regression lines (Fig. 2) indicate that the rates of oxygen consumption increase below thermoneutrality in trios us well as individuals. The regression slopes for singles, huddled trios, and separated trios arc. respectively: -0.46 (correlation coefficient. r = -0.97), -0.33 (r = -0.95). and -0.27 (r = -0.90). The slope for singles is significantly different from both trio conditions (Student’s t-test; P < 0.05). but there is no statistical difference between the slopes of the huddled and separated trios (P > 0.05). The full equations describing metabolism below thermoneutrality are:
To
PC I
Fig. 2. Oxygen consumption of single (A). separated trio (B), and huddled trio (C) Mu.7 musculus below thermoneutrality. T. = ambient temperature.
Sociality
reduces
Table 1. Oxygen consumption dard deviation, N = number
oxygen
in mice and gerbils
consumption
521
of Mus musculus. % = mean, SE = standard error of the mean. s = stanof runs, T, = ambient temperature, u;Sin = percent of singles at same
temperature SINGLES T.(C) 10 15 20 25 30
N 8 10 10 6 7
sci2SE 8.63 + 6.29 + 4.00 j, 3.28 + 2.78 +
0.35 0.27 0.36 0.46 0.31
+s 0.51 0.43 0.51 0.52 0.4 1
N 9 9 10
SEPARATED
TRIOS
x+2%? 7.26 + 0.31 5.96 _t 0.24 4.97 k 0.23
+s 0.51 0.39 0.35
sumption values than the other groups. ANOVA of Table I data for condition LB. temperature between 10~20 C revealed a significant interaction effect (F = 3.75: FIX,,,,,,,,,0 = 2.50) which is not unexpected in light of the unusually high value for separated trios at 2o’C. Nevertheless, we followed the ANOVA with the StudentkNewman-Keuls multiple range test. This analysis revealed differences between the singles mean at 10°C and singles, huddled trios, and separated trios at 20°C and huddled trios at IS’ C. Separated trios at IO’C were different only from the singles and huddled trios at 20°C. In addition to the differences noted above, the mean for huddled trios at IOC differed significantly only from huddled trios at 2o’C. These results generally confirm. the regression analysis. Significant differences appear more frequently between the singles means and other samples. particularly at the low contrasted to the high temperatures. However, the interaction of test condition and temperature suggests that we are not dealing with a simple phenomenon, and further experimentation is called for. It is well that these results are also confirmed by those for Meriorws uquiculatus.
Figure 3 compares the resting metabolism of single, huddled trio, and separated trio Mongolian gerbils. Calculated slopes for these lines are, respectively: -0.18 (r = -0.95) -0.08 (r = -0X3), and -0.07 (r = -0.81). As was the case for Mus, the highest correlation for temperature and metabolism exists within the singles condition. The slopes representing huddled and separated trios are not significantly different from one another, but both are significantly different from the slope representing the singles condition (P < 0.05). We do not have large enough samples of oxygen consumption readings at each temperature to provide data in tabular form as we did for Mus. Instead, we present a complete scatter diagram of data for separated trios in Fig. 3. There can be no doubt of the conformity of these data to those for huddled trios. The complete equation for separated trios is 4’ = -0.07s
+ 3.29.
(4)
The formula for singles and huddled trios as published by McManus & Singer (1975) are, respectively: J’ = -0.18x
+ 7.10
(5)
and y = -0.08x (the latter two rounded
+ 3.53
off to two decimal places).
(6)
HUDDLED ?/Sin 84 95 114
N 8 6 8
TRlOS
x+2SE 6.69 f 0.36 5.39 & 0.13 3.43 f 0.37
*s 0.51 0.16 0.52
“Sin 77 86 86
DISCUSSION
Comparison of Figs 2 and 3 shows that the resting metabolism of separated trio white mice is higher than the resting metabolism of huddled trios, whereas the reverse is true for Mongolian gerbils. While the data for white mice represent results from a set of experiments on similar animals, those from the gerbils do not. We tested only separated trio gerbils, and those we used were decidedly heavier than those tested by McManus & Singer (1975). Their gerbils averaged 46.1 g (singles) and 46.6 g (cagemate trios), whereas ours averaged 64.1 g. The weight-specific form of the Kleiber equation (Mb/W = 3.4 W -“.“; from McNab, 1974) predicts that basal metabolism will be approximately 8”/, lower in the larger indiGduals. Therefore, weight differences may obscure the correct relationship between the huddled and separated trio conditions. Correction for this bias still results in a close approximation of the two trio conditions and significant difference from singles. Data presented in Table I and Fig. 2 show that separated trio white mice average higher oxygen consumption than do both huddled trios and singles at 20°C. An increase of this sort was not apparent at any temperature in Meriones unguicularus,We have no definitive explanation for this response, but it may be the result of increased activity at that one ambient temperature. Mount (1960) noted that grouped pigs move away from one another as temperature rises. which at least suggests that the social mechanisms 60-
A
50# \\\\\_
40 Fs e g
30-
. .
20
--.ri.--.. C I . .... *a , ..:- .... . ..,‘....y : B -2.;
I
I
IO
I....,, l . . y.. .
1
15
20
25
Ta(“C)
Fig. 3. Oxygen consumption of single (A), separated trio (B), and huddled trio (C) Meriows wtu~riculutu,s below thermoneutrality. T. = ambient temperature. Solid circles represent individual values for separated trios.
522
ROBI-RT A. MARTIN, MAKIO FIORENTI~Vand FREIXRICX CONNORS
that act to reduce metabolism at low ambient temperatures may work in opposition as temperature rises (activity may also explain the significant condition rs. temperature interaction effect noted through ANOVA). Most authors (e.g. Prychodko. 1958; Momlt, 1960; Fedyk, 1971; McManus & Singer, 1975) note that the energetic savings due to huddling become negligible at higher ambient temperatures. The point at which the energetics of huddled and isolated animals equilibrate differs between species, but generally extrapolates near the lower limit of thermoneutrality, This point lies between 20 and 25’C for the white mice tested in this study (Fig. l), which correlates well with the temperature (20 C) at which we observed the elevated metabolic rate of separated trios. The thermal and energetic benefits of huddling behavior have been measured by the depression in resting metabolism correlated with this behavior, and it is clear that substantial savings (above 40”j0 in some species at low ambient temperatures; see McManus & Singer. 1975, for a review of savings in many small mammals) can be incurred in this way. To this point published accounts have pointed to a surface area/ mass control of metabolism. Here, we have shown that significant energetic savings can occur without physical contact. It may be that physical contact is simply one of a number of cues from conspecifics that may trigger a decrease in metabolic rate, additionally including sight. sound, smell, or trivial body heat. While we cannot prove that physical contact is not involved directly in aggregate metabolic depression, the fact that savings comparable to those counted through huddling may be promoted by means that do not include physical contact leads us to question the role of a contact factor. The concept of social facilitation as defined by Zajonc (1965) appears to be a useful model for our data. This concept was designed to describe a special learning paradigm, but can be interpreted to represent any response of an individual, behavioral or physiological. that is initiated by the presence (actual or implied) of another individual. Zajonc (1965) reviewed a number of studies which reported increased feeding activity of mammals and birds in groups relative to individual animals. To that list can be added the papers by Vetulani (1931) and Retzlaff (1939), which demonstrated that male laboratory mice gained weight faster when caged together than if kept in isolation. Prychodko (1958) additionally observed that below thermoneutrality cagemate pair and trio white mice ate less (on a weight-specific basis) than did solitary individuals. It is not possible from the design of experiments done to date with caged animals to determine if social facilitation is involved. but there are other data which support the notion that social facilitation ma) not be uncommon among vertebrates. For instance. the oxygen consumption of blennits (B/c~l/lius p/&is) increases when individuals are exposed to their mirror images (Wirtz & Davenport, 1976). Brown snakes (Storerrrc &+oJ?) respond to the presence of conspecifics and snake models with a depression of resting metabolic rate (Clausen. 1931). While many papers could be cited which demonstrate that sociality facilitates learning. we are not aware of other reports which suggest that sociality, in the absence of physical contact, facilitates a reduction in overall cellular metabolism.
Ack,,owlrdy~,ne,lrs-The research was subsidized in part by the FDU undergraduate Honors Program. We thank Drs Elizabeth Bogan and Thomas McDonald for their able direction of this program.
REFERENCES CLAUSEN H. J. (1932) The effect of aggregation
piratory
metabolism
of the brown
on the ressnake Storeriu drkuyi.
J. ceil. camp. Physiol. 8, 367-386. DABNEY M. W. & ZOLLINHOFPR R. E. (1968) The Zollin-
hofcr Manometer. a new approach to measurement of pressure change. Curoliw Tips 31. 37-38. FE~VK A. (1971) Social thermoregulation in Apodrmus,j!uricollis (Melchior. 1834). Aclu rheriol. 16. 22 I- 229. GEFKZYXSKA Z. & GEBCZYNS~~I M. (1971) Insulation properties of nest and social temperature regulation in the bank volt. Clethriowm~~.s gltrrrollrs (Schreber). Arm. Zoo/. Frnuicu 8, 104-~108. GI:BCEYNSKI M. (I 969) Social regulation of body temperature in the bank vole. Acta rhrriol. 14, 427.-440. GORES KI A. (1968)Metabolic rate and energy budget in the bank vole. Actu rlwriol. 13. 341-365. GC)RIXW A. (1969) Metabolic rate and energy budget of the striped field mouse. ilcta rhrriol. 14, 181~ 190. MARK B. A. (1974) Bioenergetics and social thermorcgulation of the white-footed mouse, Peromyscus /rucopu.s ~~owhorucrnsis. M.S. Thesis. Fairleigh Dickinson Univ.. Madison, N.J.; 39 pp. MCMANUS J. J. & SINGER C. M. (1975) Social thermoreguIation in the Mongolian gerbil, Meriones unyuiculutu.s. Bull. N.J. Arud. Sri. 20, 2625. MCNAR B. K. (1974) The energetics J. Sri. 74, 37&380.
of endotherms.
Ohio
MOUNT L. E. (1960) The influence of huddling and body size on the metabolic rate of the young pig. J. Agric. Sci. 55, 101L105.
PEAR~N 0. P. (1947) The rate of metabolism of some small mammals. Ecoloyy 28, 127-145. PEARX>N 0. P. (1960) The oxygen consumption and bioenergetics of harvest mice. Phys. ZooI. 33, 152~160. PRYCHODKO W. (1958) Effect of aggregation of laboratory mice (Mus musculus) on food intake at different temoeratures. Ecology 39, 500-503. RETZLAFF E. G. (1939) Studies in mass physiology: growth rate with the white mouse. J. exu. Zoo/. 81. 343-356. SEALANDERJ. A. JR. (1952) The relationship of nest protection and huddling to survival of Peromyscus at low temperature. Ecoloyy 33, 63-71. STANIERM. W. (1975) Effect of body weight, ambient temperature and huddling on oxygen consumption and body temperature of young mice. c‘omp. Biockem. Phy siol. 5lA, 79 82. TLRTIL R. (1972) The effect of behavioural thermoregulation on the daily metabolism of ilpodemus ugrurius (Pallas, I77 I). ilcru rhrriol. 17. 295-3 13. TROJAN P. & ~OJCIECHOWSKAB. (1968) The effect of huddling on the resting metabolism of the European common vole Microtus urwlis (Pall.). &d/I. Acud. Polonuisv Sci. 16, 107~109. VETIILANIT. (1931) Untersuchungen iiber des Wachstum der Saugetiere in Abhangigkeit von der Anzahl zusammengehaltener Tiere. Biol. Gwrrulis 7, 7 I 9X. WIE(;~RT R. G. (1961) Respiratory energy loss and activity patterns in the meadow vole, Miworus pr,ln.s~l~tr,ficus pc,nt~.s)l~urlicus. Ecology 42, 241% 253. WILSON. E. 0. (1975) Sociobiology: The New Synthesis. Harvard Univ. Press (Belknap). Cambridge. 697 pp. WIRX P. & DAVENPORT J. (1976) Increased oxygen consumption in blennies (Blrrmius pholis L.) exposed to their mirror images. J. fish Biol. 9, 67-74. Z~oxc R. B. (I 965) Social facilitation. S(~rww 149. 269-274.
of Biological
and Allied Health Sciences. Fairleigh Madison. New Jersey 07940. U.S.A.
AND
CONNORS
Dickinson
University.
The short-term resting rates of oxygen consumption of laboratory white mice (Mus IV~~.Sctrfns) and Mongolian gerbils (Meriones ur~yuicu/aru.s) were measured by closed system manometry. 2. Metabolic rates of animals tested illdividua~ly were compared to those of huddled trios and trios in which the animals were tested simultaneously but prevented from physical contact (separated trios) at tcmpcratures ranging from 9 25 C. 3. Rates of increase of weight-specific resting metabolism were greatest for animals tested individually. 4. There was no significant difference in the rates of increase of oxygen consumption between huddled and separated trios in either species. Abstract--.I.
phenomena of interest to the senior author. They are not completely comparable, but the results lead us to seriously question an accepted theoretical mechanism of mammalian energetics. For this reason we fee1 that the results should be reported now. Further. we hope that this paper will spur additional investigations into the physiological basis of sociality (sociophysiology).
Il\iTRODL:CTION Aggregation small
is a behavioral
pattern
common
to many
mammals.
Often referred to as h~iddling, it is especially apparent at low ambient temperatures. The metabolic consequences of this behavior have been studied in Apoder~us u~~rc~riu.s(Gorecki, 1968 ; Terti!, 1972). ~~~~~~~~~~~~.s .~~~~j~~~~~s (Fedyk, 197 I), ~~if~ro~ontori1~3 IN~~~~&~Ls (Pearson, 19hO), F~ro~~~yxw lrucopus (Sealander, 1952; Mark, !974), Meriotles urlgtticularus (McManus & Singer, 1975). MUS ~nusculus (Pearson, 1947 ; Prychodko, 1958; Stanier. 1973, C~~~j~~o~o~~s ~l~fr~~~i~s (Gorecki. 1969; Gebczynska & Gebczynski, 1971 ; Gebczynski, 1969). Microtus urvalis (Trojan & Wojciechowska. 196X), Miuotus p~~t~r~s~~lranicus (Wiegert, 1961). and Strs scrqfir (Mount, 1960). At low ambient temperatures aggregates demonst~te significantly lower oxygen or food consumption when compared on a weight-specific basis to animals tested individually. The cost of maintenance of core temperature also tends to decrease (Mount, 1960). The cause of these energetic and thermal benefits has been taken to be a decrease of surface area to mass ratio in aggregates. Although this may be true, another factor may be involved. As social animals. many small mammals appear to be comforted by the presence of others of the same species. This is a conclusion gained from observation of laboratory and wild animals, and is also confirmed in the literature (Wilson. 197.5). If we consider the possibility that a comfort factor is involved, then we can postulate that the decrease of energy consumption and utilization recorded by many authors may be composed of at least two components: one physical, relating to decreased surface area as an aggregate increases in mass; and one psycho-physiological, relating to the immediate presence of conspecific individuals. The purpose of this study is to test this hypothesis by comparing the oxygen consumption of three animals (a trio) under two conditions: in physical contact (huddled), and restrained from physical contact (separated). The experiments reported here are undergraduate projects and represent preliminary investigations of
MATERIALS AND METHODS Twelve laboratory white mice, strain BALBIC. and IX gerbils of both sexes were used in this study. Trios were composed of both sexes chosen at random. The gerbils derive from an initial group of LO pairs obtained from Tumblebrook Farm in 1969. This is the same laboratory population of gerbils (but not the same individuals) tested by McManus & Singer (1975). None of the females were pregnant or lactating. Weight of the white mice averaged 26.5 g, ranging from 18.5 to 34.0 e. Weirht of the gerbils averaged 6i.lg; range 55.0-75.0 g.-White-mice were hvoused individually in plastic containers. and were chosen at random to comprise test trios prior to each test. The gerbils were housed as cagemate trios. Metabolic data for the two species are not, therefore, strictly comparable. Cedar shavings were provided as bedding material. Food (Purina Lab Chow) and water were provided ud lihirtrin. Photoperiod was controlled: I6 hr light and 8 hr dark. Ambient temperature was maintained at 21 + 2’C. Experimental chambers were constructed from 3.8 1. paint cans. Three copper tubes were fashioned as entry ports in each lid. A dial thermometer was inserted in the largest. central tube (7 mm diameter). Another tube (5 mm diameter) allowed for entry of oxygen injected by a 30mI syringe. and the third (5 mm diameter) was connected in series with a manometer block (Carolma Biological Supply Company), A blank chamber (thermobarometer) was connected to the opposite side of the manometer block to complete the closed system. Brody’s Manometer Fluid acted as the volume indicator, and (indicating type) soda lime was used to absorb C02. Animals rested above the soda lime on a wire platform covered by a piece of filter paper. This system is modified from the Zollinhofer Manometer (Dabney & Zoltinhofer. 1968) and has been described elsewhere by McManus & Singer (1975). Double wire mesh separated the experimental chamber into three equal secti&. Physical contact was mandated by the placement of trios in one of the sections. but was impossible when one individual was placed in each section. 519
520
ROIXKI
A. MAKUN.
4
MARIO FIOKI WINI
and FRtUf:KI(.K
CONNOKS
IO
!I
6 t
4-
6 7
1 IO
t
I 20
I 15
!j 30
25
PC) +7 standard errors consumption of individual Mu, ~UUSXY~~UX The mean. _observed range, and number of runs ilre provided for each temperature. To
Oxygen
Ambient tcmpcrature in the cxperimcntal chumber was maintained within iO.5’C by a Magna Whirl Constant Temperature Bath containing a solution of tap wilter and salt. The experimental chamber and thermobarametric chamber were submerged during all tests to control tempcrature fluctuations. Above room temperature. water temperoturc wx maintained strictly by the water bath. Water temperature was lowered below this point by the addition of ice and maintained with il Lab Line Immersion Cooler. All animals were f~lstcd for 5 hr prior to testing. Oxygen consumption of separated and huddled trio white mice was measured at IO. IS, and 20 C. Control single white mice were tested at IO. 15, 20. 25. and 30 C. McManus & Singer (1975) provided data for single and huddled trio gerbils. We tested only separated trios. at ;1 range of temperatures between 9 and 115 C. All test individuals were allowed 30 40min to adjust to the test environment before mcasurcments were made. Testing took place between noon and midmght; generally in the curly evenings. Each oxygen consumption determination lasted between I8 and 24 min. with recordings made at 2-min intervals. Results
wcrc corrected
of the mean.
Singles;
Separated
Huddled
,’ = -0.46.~ + 13.25
(1)
?‘ = -0.27.X + 10.00
(2)
1’ = - 0.33.Y + 10.03
(3)
trios;
trios:
Table 1 presents the mean values for the three test conditions. Both trio groups generally demonstrate lower metabolic rates than individuals, although at 2O’C separated trios had higher average oxygen con-
to STP. RESL’LTS
Figure 1 depicts the temperature dependent metabolic pattern of A4us r~~usculus tested individually. Computed regression lines (Fig. 2) indicate that the rates of oxygen consumption increase below thermoneutrality in trios us well as individuals. The regression slopes for singles, huddled trios, and separated trios arc. respectively: -0.46 (correlation coefficient. r = -0.97), -0.33 (r = -0.95). and -0.27 (r = -0.90). The slope for singles is significantly different from both trio conditions (Student’s t-test; P < 0.05). but there is no statistical difference between the slopes of the huddled and separated trios (P > 0.05). The full equations describing metabolism below thermoneutrality are:
To
PC I
Fig. 2. Oxygen consumption of single (A). separated trio (B), and huddled trio (C) Mu.7 musculus below thermoneutrality. T. = ambient temperature.
Sociality
reduces
Table 1. Oxygen consumption dard deviation, N = number
oxygen
in mice and gerbils
consumption
521
of Mus musculus. % = mean, SE = standard error of the mean. s = stanof runs, T, = ambient temperature, u;Sin = percent of singles at same
temperature SINGLES T.(C) 10 15 20 25 30
N 8 10 10 6 7
sci2SE 8.63 + 6.29 + 4.00 j, 3.28 + 2.78 +
0.35 0.27 0.36 0.46 0.31
+s 0.51 0.43 0.51 0.52 0.4 1
N 9 9 10
SEPARATED
TRIOS
x+2%? 7.26 + 0.31 5.96 _t 0.24 4.97 k 0.23
+s 0.51 0.39 0.35
sumption values than the other groups. ANOVA of Table I data for condition LB. temperature between 10~20 C revealed a significant interaction effect (F = 3.75: FIX,,,,,,,,,0 = 2.50) which is not unexpected in light of the unusually high value for separated trios at 2o’C. Nevertheless, we followed the ANOVA with the StudentkNewman-Keuls multiple range test. This analysis revealed differences between the singles mean at 10°C and singles, huddled trios, and separated trios at 20°C and huddled trios at IS’ C. Separated trios at IO’C were different only from the singles and huddled trios at 20°C. In addition to the differences noted above, the mean for huddled trios at IOC differed significantly only from huddled trios at 2o’C. These results generally confirm. the regression analysis. Significant differences appear more frequently between the singles means and other samples. particularly at the low contrasted to the high temperatures. However, the interaction of test condition and temperature suggests that we are not dealing with a simple phenomenon, and further experimentation is called for. It is well that these results are also confirmed by those for Meriorws uquiculatus.
Figure 3 compares the resting metabolism of single, huddled trio, and separated trio Mongolian gerbils. Calculated slopes for these lines are, respectively: -0.18 (r = -0.95) -0.08 (r = -0X3), and -0.07 (r = -0.81). As was the case for Mus, the highest correlation for temperature and metabolism exists within the singles condition. The slopes representing huddled and separated trios are not significantly different from one another, but both are significantly different from the slope representing the singles condition (P < 0.05). We do not have large enough samples of oxygen consumption readings at each temperature to provide data in tabular form as we did for Mus. Instead, we present a complete scatter diagram of data for separated trios in Fig. 3. There can be no doubt of the conformity of these data to those for huddled trios. The complete equation for separated trios is 4’ = -0.07s
+ 3.29.
(4)
The formula for singles and huddled trios as published by McManus & Singer (1975) are, respectively: J’ = -0.18x
+ 7.10
(5)
and y = -0.08x (the latter two rounded
+ 3.53
off to two decimal places).
(6)
HUDDLED ?/Sin 84 95 114
N 8 6 8
TRlOS
x+2SE 6.69 f 0.36 5.39 & 0.13 3.43 f 0.37
*s 0.51 0.16 0.52
“Sin 77 86 86
DISCUSSION
Comparison of Figs 2 and 3 shows that the resting metabolism of separated trio white mice is higher than the resting metabolism of huddled trios, whereas the reverse is true for Mongolian gerbils. While the data for white mice represent results from a set of experiments on similar animals, those from the gerbils do not. We tested only separated trio gerbils, and those we used were decidedly heavier than those tested by McManus & Singer (1975). Their gerbils averaged 46.1 g (singles) and 46.6 g (cagemate trios), whereas ours averaged 64.1 g. The weight-specific form of the Kleiber equation (Mb/W = 3.4 W -“.“; from McNab, 1974) predicts that basal metabolism will be approximately 8”/, lower in the larger indiGduals. Therefore, weight differences may obscure the correct relationship between the huddled and separated trio conditions. Correction for this bias still results in a close approximation of the two trio conditions and significant difference from singles. Data presented in Table I and Fig. 2 show that separated trio white mice average higher oxygen consumption than do both huddled trios and singles at 20°C. An increase of this sort was not apparent at any temperature in Meriones unguicularus,We have no definitive explanation for this response, but it may be the result of increased activity at that one ambient temperature. Mount (1960) noted that grouped pigs move away from one another as temperature rises. which at least suggests that the social mechanisms 60-
A
50# \\\\\_
40 Fs e g
30-
. .
20
--.ri.--.. C I . .... *a , ..:- .... . ..,‘....y : B -2.;
I
I
IO
I....,, l . . y.. .
1
15
20
25
Ta(“C)
Fig. 3. Oxygen consumption of single (A), separated trio (B), and huddled trio (C) Meriows wtu~riculutu,s below thermoneutrality. T. = ambient temperature. Solid circles represent individual values for separated trios.
522
ROBI-RT A. MARTIN, MAKIO FIORENTI~Vand FREIXRICX CONNORS
that act to reduce metabolism at low ambient temperatures may work in opposition as temperature rises (activity may also explain the significant condition rs. temperature interaction effect noted through ANOVA). Most authors (e.g. Prychodko. 1958; Momlt, 1960; Fedyk, 1971; McManus & Singer, 1975) note that the energetic savings due to huddling become negligible at higher ambient temperatures. The point at which the energetics of huddled and isolated animals equilibrate differs between species, but generally extrapolates near the lower limit of thermoneutrality, This point lies between 20 and 25’C for the white mice tested in this study (Fig. l), which correlates well with the temperature (20 C) at which we observed the elevated metabolic rate of separated trios. The thermal and energetic benefits of huddling behavior have been measured by the depression in resting metabolism correlated with this behavior, and it is clear that substantial savings (above 40”j0 in some species at low ambient temperatures; see McManus & Singer. 1975, for a review of savings in many small mammals) can be incurred in this way. To this point published accounts have pointed to a surface area/ mass control of metabolism. Here, we have shown that significant energetic savings can occur without physical contact. It may be that physical contact is simply one of a number of cues from conspecifics that may trigger a decrease in metabolic rate, additionally including sight. sound, smell, or trivial body heat. While we cannot prove that physical contact is not involved directly in aggregate metabolic depression, the fact that savings comparable to those counted through huddling may be promoted by means that do not include physical contact leads us to question the role of a contact factor. The concept of social facilitation as defined by Zajonc (1965) appears to be a useful model for our data. This concept was designed to describe a special learning paradigm, but can be interpreted to represent any response of an individual, behavioral or physiological. that is initiated by the presence (actual or implied) of another individual. Zajonc (1965) reviewed a number of studies which reported increased feeding activity of mammals and birds in groups relative to individual animals. To that list can be added the papers by Vetulani (1931) and Retzlaff (1939), which demonstrated that male laboratory mice gained weight faster when caged together than if kept in isolation. Prychodko (1958) additionally observed that below thermoneutrality cagemate pair and trio white mice ate less (on a weight-specific basis) than did solitary individuals. It is not possible from the design of experiments done to date with caged animals to determine if social facilitation is involved. but there are other data which support the notion that social facilitation ma) not be uncommon among vertebrates. For instance. the oxygen consumption of blennits (B/c~l/lius p/&is) increases when individuals are exposed to their mirror images (Wirtz & Davenport, 1976). Brown snakes (Storerrrc &+oJ?) respond to the presence of conspecifics and snake models with a depression of resting metabolic rate (Clausen. 1931). While many papers could be cited which demonstrate that sociality facilitates learning. we are not aware of other reports which suggest that sociality, in the absence of physical contact, facilitates a reduction in overall cellular metabolism.
Ack,,owlrdy~,ne,lrs-The research was subsidized in part by the FDU undergraduate Honors Program. We thank Drs Elizabeth Bogan and Thomas McDonald for their able direction of this program.
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