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Ambient temperature effects on energetic relations in growing chicks
Physiology & Behavior, Vol. 37, pp. 203-212. Copyright©PergamonPress Ltd., 1986.Printedin the U.S.A.
0031-9384/86$3.00 + .00
Ambient Temperature Effects on Energetic Relations in Growing C h i c k s I HARLENE
HAYNE, CAROLYN ROVEE-COLLIER AND DEBRA GARGANO
D e p a r t m e n t o f Psychology, Rutgers University, N e w Brunswick, N J 08903 R e c e i v e d 7 J u n e 1985 HAYNE, H., C. ROVEE-COLLIER AND D. GARGANO. Ambient temperature effects on energetic relations in growing chicks. PHYSIOL BEHAV 37(2) 203-212, 1986.--The effects of different ambient temperature conditions on the diet selection, intake, growth, body temperature, and activity of immature domestic chicks were assessed in two experiments. In Experiment 1, the ambient temperature either remained warm during both the light and dark phases of the photoperiod, as is characteristic in laboratory settings, or was warm during the light phase and cold during the dark phase. The latter condition reflects the daily temperature pattern in natural settings. Chicks exposed to low nocturnal ambient temperatures had lower body temperatures in both phases of the photoperiod, were less active, ate more, selected a higher percentage of carbohydrate in their diets, and grew faster but were less feed-efficient than warm-reared controls. In Experiment 2, the ambient temperature was either cool in both phases of the photoperiod or cool in the light phase and warm in the dark phase. Chicks reared continuously in the cold had lower body temperatures, selected a high-carbohydrate diet, and grew faster, but both rearing groups were relatively inactive. These results show that an animal's body temperature, diet composition, food intake, feed efficiency, and activity reflect its 24-hr energy requirements and are a part of a general strategy of maximizing energy income and minimizing energy expenditure in response to energetic challenges to growth. Ambient temperature Body temperature Photoperiod Energy budget
Activity
Feeding
Diet selection
Growth
Chicks
cold ambient temperature, for example, select diets containing a higher energy:protein ratio, eat more, are less active, and maintain a lower body temperature than controls reared in a constant warm ambient temperature [25]. They also rapidly acquire an operant that turns on a heat exhaust fan [31]. In nature, where ambient temperatures are usually higher during the day than at night, young chicks minimize heat loss by maintaining close contact with the brood hen, particularly at night when temperatures drop [30]. Little is known, however, about the effect of this typical pattern of daily ambient temperature swings on their energy budgets or growth. Although chicks are active and feed exclusively in the day when the ambient temperature is warmer, for example, it is likely that these diurnal behaviors are also influenced by the thermal challenge encountered at night. If so, then the pattern of energy intake and expenditure measured in the constant thermal conditions of the laboratory would be expected to differ from the patterns seen in the variable thermal conditions characteristic of natural settings.
T H E main problem of young organisms is to grow. The amount of energy available for growth is a function of both the energy income and the energy expenditure of the organism. To the extent that calories must be diverted to maintain body temperature, for example, there is less energy available to fuel growth. Yet, most warm-blooded vertebrates are inefficient homeotherms early in ontogeny. This is due in part to immature physiological mechanisms, in part to a lack of insulation, and in part to an unfavorable surfacearea:volume ratio which results in considerable heat loss to the environment. Even precocial birds such as domestic chicks do not achieve efficient reflexive control of body temperature until sometime after the 15th day of life [2,28]. For these animals, whose solution to thermostasis is primarily behavioral, thermoregulation poses a particularly critical energetic challenge to growth. Depending upon the availability of energy sources and the demands on energy expenditure, this challenge could be met by increasing energy income, decreasing energy expenditure, or some combination of these. Chicks that are laboratory-reared in a constant
~This research was supported by NICHD Grant No. AM-31016 to George Collier and a Rutgers University Research Council Grant to C.R.C. Portions of these data were presented at the meeting of the Eastern Psychological Association, Baltimore, MD, April 1984, We thank Debbie Baer, Karen Cybulski, Linda Earley, Pamela Griesler and Johanna Jandrosovitz for their assistance in data collection, and George Collier for assistance with the preparation of diets and critical comments and suggestions on the manuscript. ~Requests for reprints should be addressed to C. Rovee-Collier, Department of Psychology, Busch Campus, Rutgers University, New Brunswick, NJ 08903.
203
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HAYNE, ROVEE-COLLIER AND GARGANO TABLE 1 PROPORTIONALCOMPONENTS, BY WEIGHT,OF EXPERIMENTALDIETS
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95.00 48.95 0 46.00 0 0.05 4.00 4.00 1.00 1.00 3.8 3.8
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Subjects Subjects were 40 straight-run White Leghorn chicks, obtained from a local supplier in a larger batch of 100 on day of hatch and distributed randomly into 4 groups of 10 each. These groups were defined in terms of the dietary and thermal conditions they would receive beginning on Day 7. Twenty chicks were reared in an ambient temperature which remained warm during both phases of the light/dark cycle (W/W), and 20 chicks were reared in the cold during the dark phase only (W/C). Within each rearing temperature condition, half of the chicks were required to compose their diet from two available food sources (Select), and half were given access to a single diet (Nonselect).
Apparatus Chicks were housed in standard Wahmann rat running wheel units. Cloacal temperatures were obtained via a YSI telethermometer (Model 43-TA, Probe Model 423) and weights, via a Torbal Balance (Model PL12D).
Procedure For the first five posthatch days chicks were reared in pairs in an ambient temperature of 35°C and on a 12-hr photoperiod (light onset at 8:30 a.m.). Chicks had free access to AGWAY medicated chick starter (21.9% protein) in each of
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FIG. 1. Daily body weights of groups reared in an ambient temperature that either remained warm in both phases of the photoperiod (W/W) or was cold in the dark phase only (W/C). The a.m. measures were taken at light onset and p.m. measures were taken immediately prior to light offset.
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METHOD
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POSTHATCH AGE (DAYS)
In the present research, we sought to determine if and how the typical pattern of cooler nights and warmer days influences diet selection, intake, body temperature, activity, and growth of immature chicks over the developmental period in which they gradually achieve efficient reflexive thermoregulation. In particular, we asked whether these behaviors are determined exclusively by the proximal thermal cues present at the time when chicks are actively feeding or whether they are influenced by information that is integrated over a longer (e.g., 24-hr) period. EXPERIMENT 1
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FIG. 2. Average daily body weights of Select and Nonselect groups in each of the two ambient temperature conditions.
two food cups, and water was continuously available. On posthatch Day 4, one of the food cups of chicks in the Select groups was filled with a soy bean oil meal diet (45% protein) and the other, with a corn meal diet (8% protein), while both cups of the Nonselect control groups were filled with a cornand soy-based diet. All diets contained adequate vitamins and minerals. These diets were previously used in diet selection studies with growing chicks [19,24] and are described in Table 1. On posthatch Day 5, chicks were randomly culled to one per cage, and beginning on posthatch Day 7, the room thermostat of the W/C groups (10 Select, 10 Nonselect) was set at 15°C one hr prior to light offset. Immediately following light onset on the next day, it was reset at the original temperature (35°C). A complete thermal transition required ap-
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FIG. 3. Dally body temperatures of chicks reared in an ambient temperature that either remained warm (W/W) or decreased during the dark phase of the photoperiod (W/C). The a.m. measures were taken at light onset and actually reflect nocturnal body temperature. The p.m. measures were taken prior to light offset and reflect diurnal body temperature.
proximately 1 hr. For the W/W groups (10 Select, 10 Nonselect), the room temperature remained at 35°C continuously. Although the thermoneutral range for chicks changes over the first 3 posthatch weeks, the higher ambient temperature (35°C) was well within the thermoneutral range for this period of development, and the lower ambient temperature (15°C) was just below thermoneutrality [5]. Running wheel activity (number of revolutions) and intake (g/cup) were recorded every 4 hr during the light phase, beginning at light onset and ending at light offset. These measures required approximately 30 min to complete. In the first and last measurement periods, body temperatures and weights were also recorded. To insure that chicks did not eat in the dark, cups were removed during the final recording period immediately preceding light offset, refilled, and returned after measures were taken following light onset. Furthermore, to prevent chicks from running in the dark, running wheel doors were closed at the conclusion of the final measurement period and reopened after measures were taken on the next day. This procedure was continued for 3 weeks, or until chicks were 28 days old. RESULTS Daily measures of body weight and body temperature were subjected to a four-way ANOVA over factors of Diet (Select, Nonselect), Light/Dark Ambient Temperature (W/W, W/C), Light Phase (2 12-hr blocks), and Days [21], with repeated measures over Days and Light phase. In a second analysis, measures of absolute nocturnal weight loss (g), relative nocturnal weight loss (g lost/p.m, body weigh0, total food intake (g), total protein intake (g), % protein in diet (total protein intake/total food intake x 100%), and feed efficiency (weight gain/total food intake) were also subjected to a four-way ANOVA over the same factors except that consumption measures across the 3 successive 4-hr periods of each 12-hr light phase were assessed instead of light- vs.
dark-phase differences. All post-hoc analyses were conducted using Duncan's multiple range test. Only significant effects (p<0.05) are reported below. Body Weight
Chicks reared in the cold during the dark phase of the photoperiod (Group W/C) gained more weight, irrespective of their diet condition, than chicks reared in a consistently warm environment (Group W/W), F(19,684)=3.93, p<0.0001. This effect, however, was solely attributable to the fact that Group W/C achieved a h i g h e r body weight during each light phase, as measured immediately prior to light offset, F(1,36)=43.58, p<0.0001 (see Fig. h "p.m."). All groups lost weight during the dark, but Group W/C lost more weight than Group W/W in each dark phase. As a result, chicks in both temperature conditions were identical in weight at the end of each dark phase (see Fig. h "a.m."). Similar 24-hr weight fluctuations have been observed in Brown Leghorn laying hens [26] and adult house sparrows [20], indicating that the pattern of nocturnal weight loss and diurnal weight gain is not restricted to either g r o w i n g or d o m e s t i c avians. Within each ambient temperature condition, chicks who composed their own diets (Group Select) grew as well as those who did not (Group Nonselect), confirming that chicks are capable of composing a diet adequate for their particular environmental conditions [ 19]. Although Group Nonselect in the W/C condition was heavier than Group Nonselect in the W/W condition, F(1,36)=5.03, p<0.03, the 24-hr weights of the corresponding Select groups (W/C, W/W) did not differ. Figure 2 illustrates the average daily growth of the four subgroups. Although the selecting chicks in the W/C condition were initially lighter than their nonselecting counterparts, by the end of the experiment, their weights did not differ. As chicks became more efficient in reflexive thermoregulation (see "Week 2"), better insulated, and less
206
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active with age, the Select groups composed diets more similar to those of Nonselect controls fed a 21.9% protein diet. / I p WlC
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Both ambient temperature groups had lower body temperatures in the dark phase (see Fig. 3: " a . m . " ) than in the light phase, F(1,36)=781.88, p <0.0001. This result is consistent with reports o f nocturnal body temperature declines in birds housed both in the laboratory under constant ambient temperature conditions [3,24] and outdoors in naturally fluctuating thermal environments [17]. However, the body temperatures o f Group W/C remained significantly lower during the light phase (see Fig. 3: " p . m . " ) than that of Group W/W, F(1,36)=2293.40, p<0.0001, even though the ambient temperature in the light phase was warm for both groups. As before, the a.m. measure, which was taken immediately after light onset, actually reflects nocturnal body temperatures. Conversely, the p.m. measure, taken immediately prior to light offset, reflects diurnal body temperatures.
Total Food Intake Total intake was greatest in both ambient temperature conditions during the first 4 hr after light onset, F(2,72)= 156.60, p<0.001. This dally distribution of food intake is consistent with field observations of a variety of wild birds [1,15]. Although the pattern of food intake was similar throughout the experiment for groups in the two ambient temperature conditions, Group W/C consumed significantly
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more than Group W/W in each measurement interval, F(1,36)=94.37, p<0.0001 (see Fig. 4). Furthermore, Nonselect groups consumed significantly more overall than Select groups, F(1,36)=5.06, p<0.03, irrespective of the ambient temperature condition.
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Absolute and Relative Nocturnal Weight Loss Although all chicks lost weight at night, Group W/C lost more both in absolute grams, F(1,36)=43.58, p<0.0001, and in percentage of body weight, F(1,36)=48.69, p<0.0001, than Group W/W, irrespective of diet condition. To determine whether the elevated food intake of chicks in Group W/C was stimulated by their greater nocturnal weight loss, a correlational analysis was performed over dally measures of both absolute and relative weight loss and food intake of all chicks during the first 4-hr measurement period following light onset. The resulting correlations were not significant, indicating that if body weight loss was a stimulus for subsequent intake, it did not account for a large portion of the variance in food intake at a time when its effect should be greatest. The lack of a significant correlation did not result from a ceiling effect on intake that restricted the range of variation; we have previously reported that growing chicks can consume a single meal in less than 2 hr every four days and maintain normal growth [18].
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Feed Efficiency
Protein Intake
Chicks reared in the cold during the dark portion of the photoperiod were less efficient than chicks reared continuously in the warm, regardless of Diet Condition, F(1,36)=29.45, p<0.0001. This reflects the added caloric requirement imposed by cold-rearing for the maintenance of body temperature. There was also a significant Room Temperature by Diet Condition interaction, F(1,36)=5.16, p <0.03. Although there was no difference between selecting and nonselecting chicks exposed to cold nocturnal temperatures, selecting chicks reared continuously in a warm ambient temperature were more feed efficient than their nonselecting controls. The feed efficiency of all groups improved over days, F(18,648)=18.41, p<0.0001; however, the feed efficiency of selecting groups improved more rapidly than that of nonselecting chicks, F(18,648)=3.12, p<0.0001, and the feed eficiency of groups reared continuously in a warm temperature improved more rapidly than that of groups reared in a cold nocturnal temperature, F(18,648)= 4.62,p <0.0001.
Although Group W/C consumed significantly more protein in absolute grams, F(1,36)=42.26, p<0.0001, this resulted from their greater overall daily intake; there was no significant difference between Groups W/C and W/W in terms of the percentage of protein in their diet. The greatest absolute amount of protein was taken during the first 4-hr period after light onset by both ambient temperature groups, irrespective of diet condition, F(2,72)=135.79, p<0.0001 (see Fig. 5: Experiment 1), when total intake was also greatest. Both Select groups, however, ate fewer total grams of protein, F(1,36)=9.77,p <0.003, and composed a diet containing a lower total percentage of protein (i.e., a higher percentage of energy) than did the corresponding Nonselect controls, F(1,36)=4.78, p<0.03. As shown in Fig. 6 (see W/W, W/C), the percentage of protein that Select groups included in their diet increased throughout the light phase, being least at the outset of each day and greatest prior to dark, F(2,72)=8.38, p<0.0005.
208
HAYNE, R O V E E - C O L L I E R AND GARGANO
The absolute amount of protein taken increased over days, F(19,684)=10.53, p<0.0001, reflecting the developmental increase in total intake. Relative protein consumption also increased with age, F(19,684)=2.10, p<0.004, indicating that chicks composed diets of increasingly greater protein content as they grew, became better insulated, and became more efficient in reflexive thermoregulation. Activity There were no significant activity differences between Select and Nonselect groups and no interactions; therefore, activity measures were collapsed over diet conditions. Chicks in both ambient temperature conditions became less active over the course of the experiment, F(19,684)=5.17, p<0.0001. However, Group W/C ran significantly less overall than did Group W/W, F(1,36)=12.99, p<0.0009, even though the ambient temperatures of the two groups were identical in the light phase, when the activity wheels were accessible (see Fig. 7: W/W, W/C). Figure 8 illustrates the distribution of running wheel activity during the light phase. Group W/C maintained a consistently low level of activity throughout the day, F(2,72)=20.81, p<0.0001, but the activity pattern of Group W/W was inversely related to its pattern of food intake. Because this pattern was not seen in Group W/C, a competingresponse analysis cannot account for this interaction. DISCUSSION
Chicks that were cold in the dark phase of the photoperiod ate more, ran less, and maintained a lower body temperature in the light phase than chicks that were warm in the dark phase; they were also less feed efficient. In addition, chicks in all rearing conditions that were allowed to compose their own diets selected a higher percentage of carbohydrate than that in the premixed "optimal" control diet. Group W/C's diurnal strategy of maximizing energy income and minimizing energy expenditure yielded growth equal to or greater than that of chicks reared in a warm nocturnal temperature. This result is consistent with previous fmdings in rats [21] and growing chickens [25,28] that cold-rearing stimulates both growth and intake. It is notable that all of the behavioral differences between the two ambient temperature groups were obtained during the light phase when environmental temperatures were identical: Access to running wheels and food was restricted to the light phase when the ambient temperature was warm, and the body weights of both groups were identical at the outset of each light phase. Given that the environmental temperature was identical for both groups during the light phase and that both groups began each day at the same body weight, the impetus for the increased intake and the decreased activity and body temperature of chicks reared in a nocturnal cold is unclear. As suggested above, chicks in the W/C condition could have been motivated by the greater absolute and/or relative amount of body weight that they lost during each dark phase relative to that lost by warm-reared chicks. However, the lack of a correlation between weight-loss measures and intake in the first 4 hr of the succeeding light phase when feeding stimulated by weight loss should be most prevalent does not lend strong support to a compensatory account. Furthermore, if chicks were motivated by their percent of body weight loss, then chicks in the W/C group should have exhibited more running-wheel activity than chicks W/W group [4, 7, 23]. Yet, activity in the W/C group was not only sup-
pressed relative to that of warm-reared controls, but it was suppressed throughout the light phase. A compensatory account of the greater total intake of the W/C group based on weight loss also does not account for the U-shaped function of intake or for the fact that Group W/C consumed significantly more than Group W/W in the final measurement period prior to dark, when Group W/C over-shot the normal body-weight curve. In spite of the fact that chicks fasted for 12 hr during the dark phase, they were not "deprived" or "depleted" in the traditional sense [7]. The body-weight losses of chicks in Group W/W never exceeded 6-7%, and the weights of chicks in Group W/C never dropped below the level of their warmreared controls. The common weights of the two groups at the outset of each day, therefore, resulted in part from their differential storage of food in the crop and gizzard in anticipation of their differential nocturnal energy requirements at the conclusion of the preceding light phase. The mechanism for this anticipatory, strategy has been described by Scanes, Campbell, and Griminger [26], who reported that in the 2.5 hr prior to dark, the crop and, to a lesser degree, the gizzard, store large quantities of feed which is subsequently metered out throughout the dark phase. The contents of the crop are depleted by 57% midway through the dark phase and by 97% 30 min prior to the light onset. In contrast, intake during the early part of the light phase is shunted past the crop, which remains empty until 2.5 hr prior to dark. A similar pattern describes the contents of the gizzard, except that it fills gradually during the light phase. Finally, it is interesting that the Select groups in both ambient temperature conditions consumed the largest amount of energy during the first 4 hr after light onset. Eating a large amount of energy in the morning may solve many problems for the chick, for example, it may facilitate a rapid increase in body temperature. However, it may also indicate the chick's anticipation of its diurnal energy demands. Omnivores eat such a way as to defend both caloric intake and the protein:energy ratio. Because the greatest proportion of their diet is carbohydrate, an effective strategy may be to consume large amounts of that component first, supplementing or "fine-tuning" the protein:energy ratio as the day wears on. The fact that Group W/C ate more, was less active, and was hypothermic relative to Group W/W even though the proximal ambient temperatures at the time that these activities occurred was identical indicates that chicks' behavior reflects their 24-hr energetic requirements rather than moment-to-moment or hour-to-hour demands (see also [26]). If this is the case, then a similar pattern of results might be obtained from chicks feeding in the cold and fasting in either a warm or a cold nocturnal environment. Given the results of Experiment 1, for example, we would predict that chicks reared continuously in the cold would eat more, run less, and grow better then chicks reared in the cold during the day and the warm at night. On the other hand, Kendeigh et al. [20] demonstrated that low nocturnal temperatures significantly increased the body weight and food intake of house sparrows, but low diurnal temperatures had little or no effect on these variables. Their data suggest that the ability of birds to regulate their intake on the basis of 24-hr energy requirements may be constrained by a day:night distribution of warm and cold ambient temperatures that approximates natural temperature patterns. This question was explored in a second study in which the pattern of temperature conditions in Experiment 1 were reversed.
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FIG. 9. The top panel illustrates the daily body weights of groups reared in an ambient temperature that either remained cold in both phases of the photoperiod (C/C) or was warm in the dark phase only (C/W). The a.m. measures were taken at light onset each day, and p.m. measures were taken immediately prior to light offset. The bottom panel illustrates the daily body weights of Select and Nonselect groups collapsed over ambient temperature conditions.
EXPERIMENT 2 METHOD
Subjects and Apparatus Subjects were 40 straight-run White Leghorn chicks, obtained as before on day of hatch in a larger batch of 100 from a local supplier. Their maintenance and rearing conditions were identical to those of Experiment 1 except that their 12-hr photoperiod began an hr earlier (7:30 a.m.), and the experimental manipulations began on posthatch day 9.
Procedure The procedure was identical in all respects to that of Experiment 1 with the exception that the ambient temperature conditions were reversed. For half of the chicks (10 Select, 10 Nonselect), the thermostat was set at 15°C at light onset and at 35°C one hr prior to light offset. For the remaining 20 chicks (10 Select, 10 Nonselec0, the room temperature remained continuously at 15°C. Thus half of the chicks were reared in the cold in both the light and dark phases of the photoperiod (C/C), while half were warm during the dark phase only (C/W).
Daily measures of body weight and body temperature were subjected to a four-way ANOVA over factors of Diet (Select, Nonselect), Light/Dark Ambient Temperature (C/C, C/W), Light Phase (2 12-hr blocks), and Days [21], with repeated measures over Light Phase and Days. Absolute nocturnal weight loss, relative nocturnal weight loss (g lost/body weight), total food intake (g), total protein intake (g), and % protein in diet (total protein intake/total food intake x 100%) were again subjected to a four-way ANOVA over factors of Diet (Select, Nonselect), Light/Dark Temperature (C/C, C/W), Time of Day (3 4-hr blocks), and Days [21], with repeated measures over Time of Day and Days. As before, all post-hoe analyses were conducted using Duncan's multiple range test, and only effects that were significant at the 0.05 level are reported.
Body Weight Chicks reared in a consistently cold environment (Group C/C), irrespective of their diet condition, tended to gain more weight during the course of the experiment than chicks reared in a warm nocturnal temperature (Group C/W), F(1,37)=3.96, p<0.054. As in Experiment 1, Both groups lost weight at night and began each succeeding day at the same body weight. However, Group C/C gained significantly more weight by the end of each light phase (see Fig. 9: Top panel). Groups that composed their own diets (Group Select) gained significantly more weight during the course of the experiment than groups that could not (Group Nonselect), irrespective of their ambient temperature condition, F(1,37)= 15.58, p<0.0003 (see Fig. 9: Bottom panel).
Body Temperature Group C/C had a significantly lower mean body temperature overall than Group C/W, irrespective of diet condition, F(1,37)=10.56, p<0.0025. As in Experiment 1, the daily body temperatures of both groups were significantly lower immediately after light onset than just prior to light offset, F(1,37) = 325.05, p <0.0001. Therefore, in both experiments diurnal variation in body temperature was keyed to the light phase even when chicks were reared in a constant ambient temperature. This finding is consistent with reports in a variety of species of birds that the highest daily body temperature is obtained during the period of greatest activity, irrespective of the proximal ambient temperature [10]. Although the body temperature of Group C/C was significantly lower than that of Group C/W at light onset, F(1,37)= 12.23, p<0.002, by light offset their temperatures did not differ. Additionally, Nonselect groups maintained significantly lower body temperatures than Select groups, irrespective of their ambient temperature condition, F(1,37)=4.97, p <0.03, suggesting that the increased energy content of the diets of the Select groups facilitated the maintenance of higher daily body temperatures (see below).
Total Food Intake Chicks increased food intake over days, F(20,719)=23.10, p<0.0001; their intake did not differ as a function of either Light/Dark Temperature or Diet Condition. As before, intake was greatest during the first 4-hr period following light onset, F(2,74)= 164.85, p<0.0001.
210
HAYNE, R O V E E - C O L L I E R AND GARGANO
Absolute and Relative Nocturnal Weight Loss
Chicks reared continuously in the cold lost more absolute grams of body weight during the dark phase of the photoperiod than chicks reared in a warm nocturnal temperature, irrespective of their diet condition, F(1,37) = 11.02, p <0.002. An analysis of relative nocturnal weight loss demonstrated that Group C/C also lost a greater percentage of its p.m. body weight in each dark phase than Group C/W, F(1,37)=14.56, p<0.0005, and Nonselect groups lost a greater percentage of their p.m. body weight than Select groups, F(1,37)=6.20, p<0.02. As in Experiment 1, there was no correlation between either weight loss measure and food intake during the first daily measurement period. Feed Efficiency
There was no main effect of either Diet or Ambient Temperature on feed efficiency and no interaction. As in Experiment 1, feed efficiency increased over days, F(19,683)=3.19, p<0.0001, and the feed efficiency of Select groups increased more rapidly than that of Nonselect groups, F(19,683)=2.03, p<0.006. Protein Intake and Relative Protein Intake
There was no significant main effect of ambient rearing temperature on either absolute or relative protein intake. Both Select groups consumed fewer absolute grams of protein, F(1,37)= 16.77,p <0.0002, and a lower percentage of dietary protein, F(1,37)=30.38, p<0.0001, than Nonselect groups, irrespective of ambient temperature condition. That Select groups feeding in the cold composed diets lower in protein and higher in carbohydrate is consistent with results obtained with mice [12] and rats [22] reared continuously in the cold, as well as with findings in Experiment 1 for chicks who were cold in the dark phase. Absolute protein intake was greatest for all groups during the first 4 hr after light onset, F(2,74)=117.21, p<0.0001, when total intake was greatest (see Fig. 5: Experiment 2). In contrast, the percent of dietary protein was greatest in the last 4 hr prior to light offset, F(2,74)=3.68, p<0.029 (see Fig. 6: C/C, C/W). This pattern of intake also mirrored that of Experiment 1. Activity
There was no main effect of either Diet or Light/Dark Temperature on activity. All chicks ran less over days, F(20,719)--20.63, p<0.001 (see Fig. 7: C/C, C/W). Activity was generally suppressed in both groups relative to activity levels typical of chicks of this age (see Experiment 1: Group w / w ; [25]). DISCUSSION
Although the intake, feed efficiency, and activity of the two groups did not differ, Group C/C maintained significantly lower body temperatures during the dark phase of the photoperiod and grew better than chicks reared in cold during the light phase only. In Experiment 1, cold during the dark phase only resulted in several diurnal adjustments (increased intake, decreased body temperature and activity). In the present study, however, the cold diurnal ambient temperature stimulated intake and suppressed activity in both groups. As a result, the superior growth of Group C/C could be attributed exclusively to their maintenance of a lower 24-hr body temperature. Although body temperature is often
viewed as a homeostatic set-point variable that is regulated within a narrow range, the present data are consistent with previous findings that body temperatures of both warmblooded [6] and cold-blooded [16] species, given certain energetic constraints, may deviate from normal range. Whether this was a passive consequence of the lower 24-hr temperature or whether the C/C Group actively defended a lower body temperature cannot be determined; however the latter is strongly implicated by the fact that the result was superior growth--a clearly adaptive outcome. Unlike the intake of chicks feeding when the ambient temperature was warm, the intake of chicks feeding diurnally in the cold appeared to be guided by proximal ambient temperature cues. Nocturnal cold did not selectively influence either absolute intake or diet composition in the present study. Although cold stimulated feeding in both C/C and C/W Groups, chicks in each group with an opportunity to control the composition of their diet in addition to the amount consumed selected a higher daily percentage of carbohydrate and grew better than the corresponding Nonselect groups. Again, however, nocturnal temperature in this experiment did not differentially influence diurnal diet selection when both groups fed in a cold environment. Thus it appears that high-carbohydrate diets are optimal for growth at lower ambient temperatures, irrespective of when in the 24-hr period the cold phase occurs. The superior growth of the chicks who were reared in nocturnal cold relative to that of chicks who presumably had an energetic conservation advantage of being warm at night suggests that growing chicks are better able to cope with ambient temperature conditions that more closely approximate natural thermal patterns than those which do not, even when the challenge is more severe. G E N E R A L DISCUSSION Although specific statistical comparisons between groups in Experiments 1 and 2 should perhaps be viewed with some caution, we matched the subjects in both experiments by age and conducted an overall analysis on the major variables in an attempt to reach some general conclusions regarding the effects of cold ambient temperatures on energetic relations in growing chicks. Chicks reared in an ambient termperature condition which most closely approximated the thermal pattern in the natural environment (W/C) grew faster, F(51,1223)=7.06, p<0.0001, than chicks in any of the other temperature conditions, while chicks reared with identical 24-hr conditions but in the reverse pattern (C/W) exhibited the most inferior growth! Chicks exposed to cold in any phase of the photoperiod (W/C, C/C, C/W) ate more, F(3,73)=3.28, p<0.03, ran less, F(3,73)=6.26, p<0.0009, and maintained lower body temperatures, F(3,73)=31.90, p<0.0001, than chicks reared continuously in a warm temperature. These results demonstrate that in the face of increased energetic demands, food intake increased, activity decreased, body temperatures decreased, diet composition changed, and food was differentially stored. For the most part, this strategy of maximizing energy income and minimizing energy expenditure resulted in growth equal to or better than that typically obtained in standard laboratory conditions of constant (warm) ambient temperatures. For chicks with cold "nights" only, this strategy completely compensated for their greater nocturnal weight loss and resulted in superior growth; for chicks with both cold "nights" and cold
E N E R G E T I C RELATIONS IN CHICKS
211
" d a y s , " this led to growth equal to that of warm-reared controls. Chicks whose " d a y s " were cold also exhibited these behavioral adjustments, but they were apparently unable to exploit any savings from warm " n i g h t s " - - a n unusual pattern of environmental temperature, and their growth was inferior to that of chicks reared under standard laboratory conditions. Several patterns of feeding behavior and activity were consistent across the ambient temperature conditions in the two experiments. Regardless of diurnal or nocturnal temperature, all groups consumed the largest proportion of carbohydrate during the first 4 hr after light onset, and the largest proportion of protein during the last 4 hr prior to light offset. A similar finding has been reported for adult rats, who consume the greatest percentage of carbohydrate at the outset of the dark phase and the greatest percentage of protein at the end of the dark phase [29]. The fact that this phenomenon is not restricted to either avians or developing organisms suggests that it is a basic feeding strategy of generalized omnivores. Given that the (a) largest proportion of the daily diet is carbohydrate, and (b) animals defend their protein:energy ratio [8], it is interesting that animals obtain the major percentage of this component first, "fine-tuning" their diet with sufficient protein in the final segment of the feeding phase. In this way, they preserve the protein:energy ratio in the face of variable supplies. It is notable that many insects, worms, and other high-protein sources exploited by birds are especially abundant at dusk. Additionally, since diets high in carbohydrate elevate body temperatures [9, 13, 14], a high-carbohydrate meal early in the day may facilitate recovery of body temperature following the nocturnal fast. To the extent that chicks in the present studies grew, we can assume that they were balancing their energy budgets effectively. Apparently the proximal cue of cold is an important but not an exclusive determinant of increased intake. Chicks feeding in a warm ambient temperature that were exposed only to nocturnal cold also increased their diurnal intake. Thus cold exposure per se, regardless of when it occurs within a 24-hr period, stimulates intake during
periods of food access. Similarly, cold in any phase of the photoperiod reduced activity--an additional component of the chick's response to thermal challenge. However, all groups, regardless of ambient temperature or diet condition, decreased running over days. Dawson and Siegel [11] reported similar results for chicks reared socially in large open pens. Thus, the present finding was not a result of individual rearing or a peculiarity of housing and probably reflects a general developmental phenomenon [27]. In conclusion, when reared in ambient temperature conditions that more closely resemble those in natural settings, growing chicks are able to alter a number of behavioral and physiological parameters in a way that maintains rapid growth. Their particular combination of strategies obviously must depend upon the behavioral options that are available. For example, given an opportunity to compose their own diet, they alter its composition and increase intake; without that option, they can only increase intake and do; these adjustments are also accompanied by alterations in factors that affect energy expenditure, e.g., activity and body temperature. However, it is more difficult for chicks to cope with ambient temperature conditions that deviate from those normally encountered in natural settings. Standard laboratory conditions not only provide such deviant conditions but also typically allow few, if any, behavioral options. As a result, laboratory animals are reared in conditions which yield less-than-maximum growth. These results lead to the conclusion that feeding behavior, dietary choice, activity, thermoregulation, and growth cannot be studied independently of one another. All contribute to the animal's energy equation, and any conclusions reached when only one factor is varied (or measured) must be limited to a particular circumscribed set of conditions. Moreover, these findings demonstrate that there is no single diet, no single activity level, body temperature, etc. that is " b e s t " under all conditions. Rather, that which is optimal depends not only on a number of environmental conditions but also on the animal's options. As these vary, so will the animal's behavioral solutions.
REFERENCES
1. Baldwin, S. P. and S. C. Kendeigh. Variations in the weight of birds. Auk 55: 416-467, 1938. 2. Barrot, H. G. and E. M. Pringle. Effect of environment on growth and feed and water consumption of chickens. J Nutr 45: 265-274, 1951. 3. Bartholomew, G. A. and W. R. Dawson. Body temperatures in California and Gambel's quail. Auk 75: 150-155, 1958. 4. Baumeister, A., W. F. Hawkins and R. L. Cromwell. Need states and activity level. Psychol Bull 61" 438--453. 5. Calder, W. A. and J. R. King. Thermal and caloric relations of birds. In: Avian Biology, Vol 2, edited by D. S. Farner and J. R. King. New York: Academic Press, 1974. 6. Carlisle, H. J. and E. Snyder. The interaction of hypothalamic self-stimulation and temperature regulation. Experientia 26: 1092-1093, 1970. 7. Collier, G. Body weight loss as a measure of motivation in hunger and thirst. Ann N Y Acad Sci 157: 594--609, 1969. 8. Collier, G. Work: A weak reinforcer. Trans N Y Acad Sci 32: 557-576, 1970. 9. Collier, G. and R. L. Squibb. Diet and activity. J Comp Physiol Psychol 64: 409-413, 1967.
10. Dawson, W. R. and J. W. Hudson. Birds. In: Comparative Physiology o f Thermoregulation, edited by G. C. Whittow. New York: Academic Press, 1970. 11. Dawson, J. S. and P. B. Siegel. Behavior patterns of chickens to ten weeks of age. Poult Sci 46: 615-622, 1967. 12. Donhoffer, S. and J. Vonotsky. The effect of environmental temperature on food selection. A m J Physiol 150: 329-333, 1947. 13. Grossman, S. P. and A. Rechtschaffen. Variations in brain temperature in relation to food intake. Physiol Behav 2: 379-383, 1967. 14. Hamilton, C. L. and W. Sheriff. Thermal behavior of the rat before and after feeding. Proc Soc Exp Bio Med 102: 746-748, 1959. 15. Helms, C. W. and W. H. Drury. Winter and migratory weight and fat field studies on some North American buntings. Bird Band 31: 1-40, 1960. 16. Huey, R. B. and M. Slatkin. Costs and benefits of lizard thermoregulation. Q Rev Biol 51: 363-384, 1976. 17. Irving, L. Nocturnal decline in the temperature of birds in cold weather. Condor 57: 362-365, 1955.
212 18. Kaufman, L. W. and G. Collier. Meal-taking by domestic chicks (Gallus gallus). Anita Behav 31: 397--403, 1983. 19. Kaufman, L. W., G. Collier and R. L. Squibb. Selection of an adequate protein-carbohydrate ratio by the domestic chick. Physiol Behav 20: 339-344, 1978. 20. Kendeigh, S. C., J. E. Kontogiannis, A. Mazac and R. Roth. Environmental regulation of food intake by birds. Bioehem Physiol 31: 941-957, 1969. 21. Kraly, F. S. and E. M. Blass. Increased feeding in rats in a low ambient temperature. In: Hunger: Basic Mechanisms and Clinical Applications, edited by D. Novin and G. Bray. New York: Raven Press, 1976. 22. Leshner, A. 1., G. H. Collier and R. L. Squibb. Dietary selfselection at cold temperatures. Physiol Behav 6: 1-3, 1971. 23. Moskowitz, M. J. Running wheel activity in the white rat as a function of combined food and water deprivation. J Comp Physiol Psychol 52: 621-625, 1959. 24. Rovee-Collier, C., B. A. Clapp and G. Collier. The economics of food choice in chicks. Physiol Behav 28: 1097-1102, 1982.
HAYNE, ROVEE-COLLIER
AND GARGANO
25. Rovee-Collier, C. and G. Collier. Dietary. Choice and Activity in the Cold. Paper presented at the International Society for Developmental Psychobiology, Hyannis, MA: October, 1983. 26. Scanes, C. G., R. Campbell and P. Griminger. The control of energy balance during egg production in the laying hen. J Nutr. in press. 27. Stahlbaum, C. C., C. Rovee-Collier, J. W. Fagen and G. Collier. Twilight activity and antipredator behavior of young fowl housed in artificial or natural light. Physiol Behav 36: 751-758, 1986. 28. Sturkie, P. D. (Ed.). Arran Physiology, 3rd edition. New York: Springer-Verlag, 1976. 29. Tempel, D. L., P. Bhakthavatsalam, G. Shor-Posner, D. Dwyer and S. F. Leibowitz. Nutrient Self-Selection at Different Periods of the Light-Dark Cycle in Free Feeding and Food Deprived Rats. Paper presented at the Eastern Psychologmal Association, Boston, MA: March 1985. 30. Wood-Gush, D. G. M. The behavior of the domestic chicken: A review of the literature. Br J Anita Behav 3: 81-110, 1955. 31. Zolman, J. F. Discrimination learning in young chickens with heat reinforcement. Psychol Rec 18: 303-309, 1968.
0031-9384/86$3.00 + .00
Ambient Temperature Effects on Energetic Relations in Growing C h i c k s I HARLENE
HAYNE, CAROLYN ROVEE-COLLIER AND DEBRA GARGANO
D e p a r t m e n t o f Psychology, Rutgers University, N e w Brunswick, N J 08903 R e c e i v e d 7 J u n e 1985 HAYNE, H., C. ROVEE-COLLIER AND D. GARGANO. Ambient temperature effects on energetic relations in growing chicks. PHYSIOL BEHAV 37(2) 203-212, 1986.--The effects of different ambient temperature conditions on the diet selection, intake, growth, body temperature, and activity of immature domestic chicks were assessed in two experiments. In Experiment 1, the ambient temperature either remained warm during both the light and dark phases of the photoperiod, as is characteristic in laboratory settings, or was warm during the light phase and cold during the dark phase. The latter condition reflects the daily temperature pattern in natural settings. Chicks exposed to low nocturnal ambient temperatures had lower body temperatures in both phases of the photoperiod, were less active, ate more, selected a higher percentage of carbohydrate in their diets, and grew faster but were less feed-efficient than warm-reared controls. In Experiment 2, the ambient temperature was either cool in both phases of the photoperiod or cool in the light phase and warm in the dark phase. Chicks reared continuously in the cold had lower body temperatures, selected a high-carbohydrate diet, and grew faster, but both rearing groups were relatively inactive. These results show that an animal's body temperature, diet composition, food intake, feed efficiency, and activity reflect its 24-hr energy requirements and are a part of a general strategy of maximizing energy income and minimizing energy expenditure in response to energetic challenges to growth. Ambient temperature Body temperature Photoperiod Energy budget
Activity
Feeding
Diet selection
Growth
Chicks
cold ambient temperature, for example, select diets containing a higher energy:protein ratio, eat more, are less active, and maintain a lower body temperature than controls reared in a constant warm ambient temperature [25]. They also rapidly acquire an operant that turns on a heat exhaust fan [31]. In nature, where ambient temperatures are usually higher during the day than at night, young chicks minimize heat loss by maintaining close contact with the brood hen, particularly at night when temperatures drop [30]. Little is known, however, about the effect of this typical pattern of daily ambient temperature swings on their energy budgets or growth. Although chicks are active and feed exclusively in the day when the ambient temperature is warmer, for example, it is likely that these diurnal behaviors are also influenced by the thermal challenge encountered at night. If so, then the pattern of energy intake and expenditure measured in the constant thermal conditions of the laboratory would be expected to differ from the patterns seen in the variable thermal conditions characteristic of natural settings.
T H E main problem of young organisms is to grow. The amount of energy available for growth is a function of both the energy income and the energy expenditure of the organism. To the extent that calories must be diverted to maintain body temperature, for example, there is less energy available to fuel growth. Yet, most warm-blooded vertebrates are inefficient homeotherms early in ontogeny. This is due in part to immature physiological mechanisms, in part to a lack of insulation, and in part to an unfavorable surfacearea:volume ratio which results in considerable heat loss to the environment. Even precocial birds such as domestic chicks do not achieve efficient reflexive control of body temperature until sometime after the 15th day of life [2,28]. For these animals, whose solution to thermostasis is primarily behavioral, thermoregulation poses a particularly critical energetic challenge to growth. Depending upon the availability of energy sources and the demands on energy expenditure, this challenge could be met by increasing energy income, decreasing energy expenditure, or some combination of these. Chicks that are laboratory-reared in a constant
~This research was supported by NICHD Grant No. AM-31016 to George Collier and a Rutgers University Research Council Grant to C.R.C. Portions of these data were presented at the meeting of the Eastern Psychological Association, Baltimore, MD, April 1984, We thank Debbie Baer, Karen Cybulski, Linda Earley, Pamela Griesler and Johanna Jandrosovitz for their assistance in data collection, and George Collier for assistance with the preparation of diets and critical comments and suggestions on the manuscript. ~Requests for reprints should be addressed to C. Rovee-Collier, Department of Psychology, Busch Campus, Rutgers University, New Brunswick, NJ 08903.
203
204
HAYNE, ROVEE-COLLIER AND GARGANO TABLE 1 PROPORTIONALCOMPONENTS, BY WEIGHT,OF EXPERIMENTALDIETS
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0 94.90 0 4.00 1.00 3.8
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65 50
Subjects Subjects were 40 straight-run White Leghorn chicks, obtained from a local supplier in a larger batch of 100 on day of hatch and distributed randomly into 4 groups of 10 each. These groups were defined in terms of the dietary and thermal conditions they would receive beginning on Day 7. Twenty chicks were reared in an ambient temperature which remained warm during both phases of the light/dark cycle (W/W), and 20 chicks were reared in the cold during the dark phase only (W/C). Within each rearing temperature condition, half of the chicks were required to compose their diet from two available food sources (Select), and half were given access to a single diet (Nonselect).
Apparatus Chicks were housed in standard Wahmann rat running wheel units. Cloacal temperatures were obtained via a YSI telethermometer (Model 43-TA, Probe Model 423) and weights, via a Torbal Balance (Model PL12D).
Procedure For the first five posthatch days chicks were reared in pairs in an ambient temperature of 35°C and on a 12-hr photoperiod (light onset at 8:30 a.m.). Chicks had free access to AGWAY medicated chick starter (21.9% protein) in each of
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FIG. 1. Daily body weights of groups reared in an ambient temperature that either remained warm in both phases of the photoperiod (W/W) or was cold in the dark phase only (W/C). The a.m. measures were taken at light onset and p.m. measures were taken immediately prior to light offset.
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POSTHATCH AGE (DAYS)
In the present research, we sought to determine if and how the typical pattern of cooler nights and warmer days influences diet selection, intake, body temperature, activity, and growth of immature chicks over the developmental period in which they gradually achieve efficient reflexive thermoregulation. In particular, we asked whether these behaviors are determined exclusively by the proximal thermal cues present at the time when chicks are actively feeding or whether they are influenced by information that is integrated over a longer (e.g., 24-hr) period. EXPERIMENT 1
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two food cups, and water was continuously available. On posthatch Day 4, one of the food cups of chicks in the Select groups was filled with a soy bean oil meal diet (45% protein) and the other, with a corn meal diet (8% protein), while both cups of the Nonselect control groups were filled with a cornand soy-based diet. All diets contained adequate vitamins and minerals. These diets were previously used in diet selection studies with growing chicks [19,24] and are described in Table 1. On posthatch Day 5, chicks were randomly culled to one per cage, and beginning on posthatch Day 7, the room thermostat of the W/C groups (10 Select, 10 Nonselect) was set at 15°C one hr prior to light offset. Immediately following light onset on the next day, it was reset at the original temperature (35°C). A complete thermal transition required ap-
ENERGETIC RELATIONS IN CHICKS
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FIG. 3. Dally body temperatures of chicks reared in an ambient temperature that either remained warm (W/W) or decreased during the dark phase of the photoperiod (W/C). The a.m. measures were taken at light onset and actually reflect nocturnal body temperature. The p.m. measures were taken prior to light offset and reflect diurnal body temperature.
proximately 1 hr. For the W/W groups (10 Select, 10 Nonselect), the room temperature remained at 35°C continuously. Although the thermoneutral range for chicks changes over the first 3 posthatch weeks, the higher ambient temperature (35°C) was well within the thermoneutral range for this period of development, and the lower ambient temperature (15°C) was just below thermoneutrality [5]. Running wheel activity (number of revolutions) and intake (g/cup) were recorded every 4 hr during the light phase, beginning at light onset and ending at light offset. These measures required approximately 30 min to complete. In the first and last measurement periods, body temperatures and weights were also recorded. To insure that chicks did not eat in the dark, cups were removed during the final recording period immediately preceding light offset, refilled, and returned after measures were taken following light onset. Furthermore, to prevent chicks from running in the dark, running wheel doors were closed at the conclusion of the final measurement period and reopened after measures were taken on the next day. This procedure was continued for 3 weeks, or until chicks were 28 days old. RESULTS Daily measures of body weight and body temperature were subjected to a four-way ANOVA over factors of Diet (Select, Nonselect), Light/Dark Ambient Temperature (W/W, W/C), Light Phase (2 12-hr blocks), and Days [21], with repeated measures over Days and Light phase. In a second analysis, measures of absolute nocturnal weight loss (g), relative nocturnal weight loss (g lost/p.m, body weigh0, total food intake (g), total protein intake (g), % protein in diet (total protein intake/total food intake x 100%), and feed efficiency (weight gain/total food intake) were also subjected to a four-way ANOVA over the same factors except that consumption measures across the 3 successive 4-hr periods of each 12-hr light phase were assessed instead of light- vs.
dark-phase differences. All post-hoc analyses were conducted using Duncan's multiple range test. Only significant effects (p<0.05) are reported below. Body Weight
Chicks reared in the cold during the dark phase of the photoperiod (Group W/C) gained more weight, irrespective of their diet condition, than chicks reared in a consistently warm environment (Group W/W), F(19,684)=3.93, p<0.0001. This effect, however, was solely attributable to the fact that Group W/C achieved a h i g h e r body weight during each light phase, as measured immediately prior to light offset, F(1,36)=43.58, p<0.0001 (see Fig. h "p.m."). All groups lost weight during the dark, but Group W/C lost more weight than Group W/W in each dark phase. As a result, chicks in both temperature conditions were identical in weight at the end of each dark phase (see Fig. h "a.m."). Similar 24-hr weight fluctuations have been observed in Brown Leghorn laying hens [26] and adult house sparrows [20], indicating that the pattern of nocturnal weight loss and diurnal weight gain is not restricted to either g r o w i n g or d o m e s t i c avians. Within each ambient temperature condition, chicks who composed their own diets (Group Select) grew as well as those who did not (Group Nonselect), confirming that chicks are capable of composing a diet adequate for their particular environmental conditions [ 19]. Although Group Nonselect in the W/C condition was heavier than Group Nonselect in the W/W condition, F(1,36)=5.03, p<0.03, the 24-hr weights of the corresponding Select groups (W/C, W/W) did not differ. Figure 2 illustrates the average daily growth of the four subgroups. Although the selecting chicks in the W/C condition were initially lighter than their nonselecting counterparts, by the end of the experiment, their weights did not differ. As chicks became more efficient in reflexive thermoregulation (see "Week 2"), better insulated, and less
206
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Both ambient temperature groups had lower body temperatures in the dark phase (see Fig. 3: " a . m . " ) than in the light phase, F(1,36)=781.88, p <0.0001. This result is consistent with reports o f nocturnal body temperature declines in birds housed both in the laboratory under constant ambient temperature conditions [3,24] and outdoors in naturally fluctuating thermal environments [17]. However, the body temperatures o f Group W/C remained significantly lower during the light phase (see Fig. 3: " p . m . " ) than that of Group W/W, F(1,36)=2293.40, p<0.0001, even though the ambient temperature in the light phase was warm for both groups. As before, the a.m. measure, which was taken immediately after light onset, actually reflects nocturnal body temperatures. Conversely, the p.m. measure, taken immediately prior to light offset, reflects diurnal body temperatures.
Total Food Intake Total intake was greatest in both ambient temperature conditions during the first 4 hr after light onset, F(2,72)= 156.60, p<0.001. This dally distribution of food intake is consistent with field observations of a variety of wild birds [1,15]. Although the pattern of food intake was similar throughout the experiment for groups in the two ambient temperature conditions, Group W/C consumed significantly
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Feed Efficiency
Protein Intake
Chicks reared in the cold during the dark portion of the photoperiod were less efficient than chicks reared continuously in the warm, regardless of Diet Condition, F(1,36)=29.45, p<0.0001. This reflects the added caloric requirement imposed by cold-rearing for the maintenance of body temperature. There was also a significant Room Temperature by Diet Condition interaction, F(1,36)=5.16, p <0.03. Although there was no difference between selecting and nonselecting chicks exposed to cold nocturnal temperatures, selecting chicks reared continuously in a warm ambient temperature were more feed efficient than their nonselecting controls. The feed efficiency of all groups improved over days, F(18,648)=18.41, p<0.0001; however, the feed efficiency of selecting groups improved more rapidly than that of nonselecting chicks, F(18,648)=3.12, p<0.0001, and the feed eficiency of groups reared continuously in a warm temperature improved more rapidly than that of groups reared in a cold nocturnal temperature, F(18,648)= 4.62,p <0.0001.
Although Group W/C consumed significantly more protein in absolute grams, F(1,36)=42.26, p<0.0001, this resulted from their greater overall daily intake; there was no significant difference between Groups W/C and W/W in terms of the percentage of protein in their diet. The greatest absolute amount of protein was taken during the first 4-hr period after light onset by both ambient temperature groups, irrespective of diet condition, F(2,72)=135.79, p<0.0001 (see Fig. 5: Experiment 1), when total intake was also greatest. Both Select groups, however, ate fewer total grams of protein, F(1,36)=9.77,p <0.003, and composed a diet containing a lower total percentage of protein (i.e., a higher percentage of energy) than did the corresponding Nonselect controls, F(1,36)=4.78, p<0.03. As shown in Fig. 6 (see W/W, W/C), the percentage of protein that Select groups included in their diet increased throughout the light phase, being least at the outset of each day and greatest prior to dark, F(2,72)=8.38, p<0.0005.
208
HAYNE, R O V E E - C O L L I E R AND GARGANO
The absolute amount of protein taken increased over days, F(19,684)=10.53, p<0.0001, reflecting the developmental increase in total intake. Relative protein consumption also increased with age, F(19,684)=2.10, p<0.004, indicating that chicks composed diets of increasingly greater protein content as they grew, became better insulated, and became more efficient in reflexive thermoregulation. Activity There were no significant activity differences between Select and Nonselect groups and no interactions; therefore, activity measures were collapsed over diet conditions. Chicks in both ambient temperature conditions became less active over the course of the experiment, F(19,684)=5.17, p<0.0001. However, Group W/C ran significantly less overall than did Group W/W, F(1,36)=12.99, p<0.0009, even though the ambient temperatures of the two groups were identical in the light phase, when the activity wheels were accessible (see Fig. 7: W/W, W/C). Figure 8 illustrates the distribution of running wheel activity during the light phase. Group W/C maintained a consistently low level of activity throughout the day, F(2,72)=20.81, p<0.0001, but the activity pattern of Group W/W was inversely related to its pattern of food intake. Because this pattern was not seen in Group W/C, a competingresponse analysis cannot account for this interaction. DISCUSSION
Chicks that were cold in the dark phase of the photoperiod ate more, ran less, and maintained a lower body temperature in the light phase than chicks that were warm in the dark phase; they were also less feed efficient. In addition, chicks in all rearing conditions that were allowed to compose their own diets selected a higher percentage of carbohydrate than that in the premixed "optimal" control diet. Group W/C's diurnal strategy of maximizing energy income and minimizing energy expenditure yielded growth equal to or greater than that of chicks reared in a warm nocturnal temperature. This result is consistent with previous fmdings in rats [21] and growing chickens [25,28] that cold-rearing stimulates both growth and intake. It is notable that all of the behavioral differences between the two ambient temperature groups were obtained during the light phase when environmental temperatures were identical: Access to running wheels and food was restricted to the light phase when the ambient temperature was warm, and the body weights of both groups were identical at the outset of each light phase. Given that the environmental temperature was identical for both groups during the light phase and that both groups began each day at the same body weight, the impetus for the increased intake and the decreased activity and body temperature of chicks reared in a nocturnal cold is unclear. As suggested above, chicks in the W/C condition could have been motivated by the greater absolute and/or relative amount of body weight that they lost during each dark phase relative to that lost by warm-reared chicks. However, the lack of a correlation between weight-loss measures and intake in the first 4 hr of the succeeding light phase when feeding stimulated by weight loss should be most prevalent does not lend strong support to a compensatory account. Furthermore, if chicks were motivated by their percent of body weight loss, then chicks in the W/C group should have exhibited more running-wheel activity than chicks W/W group [4, 7, 23]. Yet, activity in the W/C group was not only sup-
pressed relative to that of warm-reared controls, but it was suppressed throughout the light phase. A compensatory account of the greater total intake of the W/C group based on weight loss also does not account for the U-shaped function of intake or for the fact that Group W/C consumed significantly more than Group W/W in the final measurement period prior to dark, when Group W/C over-shot the normal body-weight curve. In spite of the fact that chicks fasted for 12 hr during the dark phase, they were not "deprived" or "depleted" in the traditional sense [7]. The body-weight losses of chicks in Group W/W never exceeded 6-7%, and the weights of chicks in Group W/C never dropped below the level of their warmreared controls. The common weights of the two groups at the outset of each day, therefore, resulted in part from their differential storage of food in the crop and gizzard in anticipation of their differential nocturnal energy requirements at the conclusion of the preceding light phase. The mechanism for this anticipatory, strategy has been described by Scanes, Campbell, and Griminger [26], who reported that in the 2.5 hr prior to dark, the crop and, to a lesser degree, the gizzard, store large quantities of feed which is subsequently metered out throughout the dark phase. The contents of the crop are depleted by 57% midway through the dark phase and by 97% 30 min prior to the light onset. In contrast, intake during the early part of the light phase is shunted past the crop, which remains empty until 2.5 hr prior to dark. A similar pattern describes the contents of the gizzard, except that it fills gradually during the light phase. Finally, it is interesting that the Select groups in both ambient temperature conditions consumed the largest amount of energy during the first 4 hr after light onset. Eating a large amount of energy in the morning may solve many problems for the chick, for example, it may facilitate a rapid increase in body temperature. However, it may also indicate the chick's anticipation of its diurnal energy demands. Omnivores eat such a way as to defend both caloric intake and the protein:energy ratio. Because the greatest proportion of their diet is carbohydrate, an effective strategy may be to consume large amounts of that component first, supplementing or "fine-tuning" the protein:energy ratio as the day wears on. The fact that Group W/C ate more, was less active, and was hypothermic relative to Group W/W even though the proximal ambient temperatures at the time that these activities occurred was identical indicates that chicks' behavior reflects their 24-hr energetic requirements rather than moment-to-moment or hour-to-hour demands (see also [26]). If this is the case, then a similar pattern of results might be obtained from chicks feeding in the cold and fasting in either a warm or a cold nocturnal environment. Given the results of Experiment 1, for example, we would predict that chicks reared continuously in the cold would eat more, run less, and grow better then chicks reared in the cold during the day and the warm at night. On the other hand, Kendeigh et al. [20] demonstrated that low nocturnal temperatures significantly increased the body weight and food intake of house sparrows, but low diurnal temperatures had little or no effect on these variables. Their data suggest that the ability of birds to regulate their intake on the basis of 24-hr energy requirements may be constrained by a day:night distribution of warm and cold ambient temperatures that approximates natural temperature patterns. This question was explored in a second study in which the pattern of temperature conditions in Experiment 1 were reversed.
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FIG. 9. The top panel illustrates the daily body weights of groups reared in an ambient temperature that either remained cold in both phases of the photoperiod (C/C) or was warm in the dark phase only (C/W). The a.m. measures were taken at light onset each day, and p.m. measures were taken immediately prior to light offset. The bottom panel illustrates the daily body weights of Select and Nonselect groups collapsed over ambient temperature conditions.
EXPERIMENT 2 METHOD
Subjects and Apparatus Subjects were 40 straight-run White Leghorn chicks, obtained as before on day of hatch in a larger batch of 100 from a local supplier. Their maintenance and rearing conditions were identical to those of Experiment 1 except that their 12-hr photoperiod began an hr earlier (7:30 a.m.), and the experimental manipulations began on posthatch day 9.
Procedure The procedure was identical in all respects to that of Experiment 1 with the exception that the ambient temperature conditions were reversed. For half of the chicks (10 Select, 10 Nonselect), the thermostat was set at 15°C at light onset and at 35°C one hr prior to light offset. For the remaining 20 chicks (10 Select, 10 Nonselec0, the room temperature remained continuously at 15°C. Thus half of the chicks were reared in the cold in both the light and dark phases of the photoperiod (C/C), while half were warm during the dark phase only (C/W).
Daily measures of body weight and body temperature were subjected to a four-way ANOVA over factors of Diet (Select, Nonselect), Light/Dark Ambient Temperature (C/C, C/W), Light Phase (2 12-hr blocks), and Days [21], with repeated measures over Light Phase and Days. Absolute nocturnal weight loss, relative nocturnal weight loss (g lost/body weight), total food intake (g), total protein intake (g), and % protein in diet (total protein intake/total food intake x 100%) were again subjected to a four-way ANOVA over factors of Diet (Select, Nonselect), Light/Dark Temperature (C/C, C/W), Time of Day (3 4-hr blocks), and Days [21], with repeated measures over Time of Day and Days. As before, all post-hoe analyses were conducted using Duncan's multiple range test, and only effects that were significant at the 0.05 level are reported.
Body Weight Chicks reared in a consistently cold environment (Group C/C), irrespective of their diet condition, tended to gain more weight during the course of the experiment than chicks reared in a warm nocturnal temperature (Group C/W), F(1,37)=3.96, p<0.054. As in Experiment 1, Both groups lost weight at night and began each succeeding day at the same body weight. However, Group C/C gained significantly more weight by the end of each light phase (see Fig. 9: Top panel). Groups that composed their own diets (Group Select) gained significantly more weight during the course of the experiment than groups that could not (Group Nonselect), irrespective of their ambient temperature condition, F(1,37)= 15.58, p<0.0003 (see Fig. 9: Bottom panel).
Body Temperature Group C/C had a significantly lower mean body temperature overall than Group C/W, irrespective of diet condition, F(1,37)=10.56, p<0.0025. As in Experiment 1, the daily body temperatures of both groups were significantly lower immediately after light onset than just prior to light offset, F(1,37) = 325.05, p <0.0001. Therefore, in both experiments diurnal variation in body temperature was keyed to the light phase even when chicks were reared in a constant ambient temperature. This finding is consistent with reports in a variety of species of birds that the highest daily body temperature is obtained during the period of greatest activity, irrespective of the proximal ambient temperature [10]. Although the body temperature of Group C/C was significantly lower than that of Group C/W at light onset, F(1,37)= 12.23, p<0.002, by light offset their temperatures did not differ. Additionally, Nonselect groups maintained significantly lower body temperatures than Select groups, irrespective of their ambient temperature condition, F(1,37)=4.97, p <0.03, suggesting that the increased energy content of the diets of the Select groups facilitated the maintenance of higher daily body temperatures (see below).
Total Food Intake Chicks increased food intake over days, F(20,719)=23.10, p<0.0001; their intake did not differ as a function of either Light/Dark Temperature or Diet Condition. As before, intake was greatest during the first 4-hr period following light onset, F(2,74)= 164.85, p<0.0001.
210
HAYNE, R O V E E - C O L L I E R AND GARGANO
Absolute and Relative Nocturnal Weight Loss
Chicks reared continuously in the cold lost more absolute grams of body weight during the dark phase of the photoperiod than chicks reared in a warm nocturnal temperature, irrespective of their diet condition, F(1,37) = 11.02, p <0.002. An analysis of relative nocturnal weight loss demonstrated that Group C/C also lost a greater percentage of its p.m. body weight in each dark phase than Group C/W, F(1,37)=14.56, p<0.0005, and Nonselect groups lost a greater percentage of their p.m. body weight than Select groups, F(1,37)=6.20, p<0.02. As in Experiment 1, there was no correlation between either weight loss measure and food intake during the first daily measurement period. Feed Efficiency
There was no main effect of either Diet or Ambient Temperature on feed efficiency and no interaction. As in Experiment 1, feed efficiency increased over days, F(19,683)=3.19, p<0.0001, and the feed efficiency of Select groups increased more rapidly than that of Nonselect groups, F(19,683)=2.03, p<0.006. Protein Intake and Relative Protein Intake
There was no significant main effect of ambient rearing temperature on either absolute or relative protein intake. Both Select groups consumed fewer absolute grams of protein, F(1,37)= 16.77,p <0.0002, and a lower percentage of dietary protein, F(1,37)=30.38, p<0.0001, than Nonselect groups, irrespective of ambient temperature condition. That Select groups feeding in the cold composed diets lower in protein and higher in carbohydrate is consistent with results obtained with mice [12] and rats [22] reared continuously in the cold, as well as with findings in Experiment 1 for chicks who were cold in the dark phase. Absolute protein intake was greatest for all groups during the first 4 hr after light onset, F(2,74)=117.21, p<0.0001, when total intake was greatest (see Fig. 5: Experiment 2). In contrast, the percent of dietary protein was greatest in the last 4 hr prior to light offset, F(2,74)=3.68, p<0.029 (see Fig. 6: C/C, C/W). This pattern of intake also mirrored that of Experiment 1. Activity
There was no main effect of either Diet or Light/Dark Temperature on activity. All chicks ran less over days, F(20,719)--20.63, p<0.001 (see Fig. 7: C/C, C/W). Activity was generally suppressed in both groups relative to activity levels typical of chicks of this age (see Experiment 1: Group w / w ; [25]). DISCUSSION
Although the intake, feed efficiency, and activity of the two groups did not differ, Group C/C maintained significantly lower body temperatures during the dark phase of the photoperiod and grew better than chicks reared in cold during the light phase only. In Experiment 1, cold during the dark phase only resulted in several diurnal adjustments (increased intake, decreased body temperature and activity). In the present study, however, the cold diurnal ambient temperature stimulated intake and suppressed activity in both groups. As a result, the superior growth of Group C/C could be attributed exclusively to their maintenance of a lower 24-hr body temperature. Although body temperature is often
viewed as a homeostatic set-point variable that is regulated within a narrow range, the present data are consistent with previous findings that body temperatures of both warmblooded [6] and cold-blooded [16] species, given certain energetic constraints, may deviate from normal range. Whether this was a passive consequence of the lower 24-hr temperature or whether the C/C Group actively defended a lower body temperature cannot be determined; however the latter is strongly implicated by the fact that the result was superior growth--a clearly adaptive outcome. Unlike the intake of chicks feeding when the ambient temperature was warm, the intake of chicks feeding diurnally in the cold appeared to be guided by proximal ambient temperature cues. Nocturnal cold did not selectively influence either absolute intake or diet composition in the present study. Although cold stimulated feeding in both C/C and C/W Groups, chicks in each group with an opportunity to control the composition of their diet in addition to the amount consumed selected a higher daily percentage of carbohydrate and grew better than the corresponding Nonselect groups. Again, however, nocturnal temperature in this experiment did not differentially influence diurnal diet selection when both groups fed in a cold environment. Thus it appears that high-carbohydrate diets are optimal for growth at lower ambient temperatures, irrespective of when in the 24-hr period the cold phase occurs. The superior growth of the chicks who were reared in nocturnal cold relative to that of chicks who presumably had an energetic conservation advantage of being warm at night suggests that growing chicks are better able to cope with ambient temperature conditions that more closely approximate natural thermal patterns than those which do not, even when the challenge is more severe. G E N E R A L DISCUSSION Although specific statistical comparisons between groups in Experiments 1 and 2 should perhaps be viewed with some caution, we matched the subjects in both experiments by age and conducted an overall analysis on the major variables in an attempt to reach some general conclusions regarding the effects of cold ambient temperatures on energetic relations in growing chicks. Chicks reared in an ambient termperature condition which most closely approximated the thermal pattern in the natural environment (W/C) grew faster, F(51,1223)=7.06, p<0.0001, than chicks in any of the other temperature conditions, while chicks reared with identical 24-hr conditions but in the reverse pattern (C/W) exhibited the most inferior growth! Chicks exposed to cold in any phase of the photoperiod (W/C, C/C, C/W) ate more, F(3,73)=3.28, p<0.03, ran less, F(3,73)=6.26, p<0.0009, and maintained lower body temperatures, F(3,73)=31.90, p<0.0001, than chicks reared continuously in a warm temperature. These results demonstrate that in the face of increased energetic demands, food intake increased, activity decreased, body temperatures decreased, diet composition changed, and food was differentially stored. For the most part, this strategy of maximizing energy income and minimizing energy expenditure resulted in growth equal to or better than that typically obtained in standard laboratory conditions of constant (warm) ambient temperatures. For chicks with cold "nights" only, this strategy completely compensated for their greater nocturnal weight loss and resulted in superior growth; for chicks with both cold "nights" and cold
E N E R G E T I C RELATIONS IN CHICKS
211
" d a y s , " this led to growth equal to that of warm-reared controls. Chicks whose " d a y s " were cold also exhibited these behavioral adjustments, but they were apparently unable to exploit any savings from warm " n i g h t s " - - a n unusual pattern of environmental temperature, and their growth was inferior to that of chicks reared under standard laboratory conditions. Several patterns of feeding behavior and activity were consistent across the ambient temperature conditions in the two experiments. Regardless of diurnal or nocturnal temperature, all groups consumed the largest proportion of carbohydrate during the first 4 hr after light onset, and the largest proportion of protein during the last 4 hr prior to light offset. A similar finding has been reported for adult rats, who consume the greatest percentage of carbohydrate at the outset of the dark phase and the greatest percentage of protein at the end of the dark phase [29]. The fact that this phenomenon is not restricted to either avians or developing organisms suggests that it is a basic feeding strategy of generalized omnivores. Given that the (a) largest proportion of the daily diet is carbohydrate, and (b) animals defend their protein:energy ratio [8], it is interesting that animals obtain the major percentage of this component first, "fine-tuning" their diet with sufficient protein in the final segment of the feeding phase. In this way, they preserve the protein:energy ratio in the face of variable supplies. It is notable that many insects, worms, and other high-protein sources exploited by birds are especially abundant at dusk. Additionally, since diets high in carbohydrate elevate body temperatures [9, 13, 14], a high-carbohydrate meal early in the day may facilitate recovery of body temperature following the nocturnal fast. To the extent that chicks in the present studies grew, we can assume that they were balancing their energy budgets effectively. Apparently the proximal cue of cold is an important but not an exclusive determinant of increased intake. Chicks feeding in a warm ambient temperature that were exposed only to nocturnal cold also increased their diurnal intake. Thus cold exposure per se, regardless of when it occurs within a 24-hr period, stimulates intake during
periods of food access. Similarly, cold in any phase of the photoperiod reduced activity--an additional component of the chick's response to thermal challenge. However, all groups, regardless of ambient temperature or diet condition, decreased running over days. Dawson and Siegel [11] reported similar results for chicks reared socially in large open pens. Thus, the present finding was not a result of individual rearing or a peculiarity of housing and probably reflects a general developmental phenomenon [27]. In conclusion, when reared in ambient temperature conditions that more closely resemble those in natural settings, growing chicks are able to alter a number of behavioral and physiological parameters in a way that maintains rapid growth. Their particular combination of strategies obviously must depend upon the behavioral options that are available. For example, given an opportunity to compose their own diet, they alter its composition and increase intake; without that option, they can only increase intake and do; these adjustments are also accompanied by alterations in factors that affect energy expenditure, e.g., activity and body temperature. However, it is more difficult for chicks to cope with ambient temperature conditions that deviate from those normally encountered in natural settings. Standard laboratory conditions not only provide such deviant conditions but also typically allow few, if any, behavioral options. As a result, laboratory animals are reared in conditions which yield less-than-maximum growth. These results lead to the conclusion that feeding behavior, dietary choice, activity, thermoregulation, and growth cannot be studied independently of one another. All contribute to the animal's energy equation, and any conclusions reached when only one factor is varied (or measured) must be limited to a particular circumscribed set of conditions. Moreover, these findings demonstrate that there is no single diet, no single activity level, body temperature, etc. that is " b e s t " under all conditions. Rather, that which is optimal depends not only on a number of environmental conditions but also on the animal's options. As these vary, so will the animal's behavioral solutions.
REFERENCES
1. Baldwin, S. P. and S. C. Kendeigh. Variations in the weight of birds. Auk 55: 416-467, 1938. 2. Barrot, H. G. and E. M. Pringle. Effect of environment on growth and feed and water consumption of chickens. J Nutr 45: 265-274, 1951. 3. Bartholomew, G. A. and W. R. Dawson. Body temperatures in California and Gambel's quail. Auk 75: 150-155, 1958. 4. Baumeister, A., W. F. Hawkins and R. L. Cromwell. Need states and activity level. Psychol Bull 61" 438--453. 5. Calder, W. A. and J. R. King. Thermal and caloric relations of birds. In: Avian Biology, Vol 2, edited by D. S. Farner and J. R. King. New York: Academic Press, 1974. 6. Carlisle, H. J. and E. Snyder. The interaction of hypothalamic self-stimulation and temperature regulation. Experientia 26: 1092-1093, 1970. 7. Collier, G. Body weight loss as a measure of motivation in hunger and thirst. Ann N Y Acad Sci 157: 594--609, 1969. 8. Collier, G. Work: A weak reinforcer. Trans N Y Acad Sci 32: 557-576, 1970. 9. Collier, G. and R. L. Squibb. Diet and activity. J Comp Physiol Psychol 64: 409-413, 1967.
10. Dawson, W. R. and J. W. Hudson. Birds. In: Comparative Physiology o f Thermoregulation, edited by G. C. Whittow. New York: Academic Press, 1970. 11. Dawson, J. S. and P. B. Siegel. Behavior patterns of chickens to ten weeks of age. Poult Sci 46: 615-622, 1967. 12. Donhoffer, S. and J. Vonotsky. The effect of environmental temperature on food selection. A m J Physiol 150: 329-333, 1947. 13. Grossman, S. P. and A. Rechtschaffen. Variations in brain temperature in relation to food intake. Physiol Behav 2: 379-383, 1967. 14. Hamilton, C. L. and W. Sheriff. Thermal behavior of the rat before and after feeding. Proc Soc Exp Bio Med 102: 746-748, 1959. 15. Helms, C. W. and W. H. Drury. Winter and migratory weight and fat field studies on some North American buntings. Bird Band 31: 1-40, 1960. 16. Huey, R. B. and M. Slatkin. Costs and benefits of lizard thermoregulation. Q Rev Biol 51: 363-384, 1976. 17. Irving, L. Nocturnal decline in the temperature of birds in cold weather. Condor 57: 362-365, 1955.
212 18. Kaufman, L. W. and G. Collier. Meal-taking by domestic chicks (Gallus gallus). Anita Behav 31: 397--403, 1983. 19. Kaufman, L. W., G. Collier and R. L. Squibb. Selection of an adequate protein-carbohydrate ratio by the domestic chick. Physiol Behav 20: 339-344, 1978. 20. Kendeigh, S. C., J. E. Kontogiannis, A. Mazac and R. Roth. Environmental regulation of food intake by birds. Bioehem Physiol 31: 941-957, 1969. 21. Kraly, F. S. and E. M. Blass. Increased feeding in rats in a low ambient temperature. In: Hunger: Basic Mechanisms and Clinical Applications, edited by D. Novin and G. Bray. New York: Raven Press, 1976. 22. Leshner, A. 1., G. H. Collier and R. L. Squibb. Dietary selfselection at cold temperatures. Physiol Behav 6: 1-3, 1971. 23. Moskowitz, M. J. Running wheel activity in the white rat as a function of combined food and water deprivation. J Comp Physiol Psychol 52: 621-625, 1959. 24. Rovee-Collier, C., B. A. Clapp and G. Collier. The economics of food choice in chicks. Physiol Behav 28: 1097-1102, 1982.
HAYNE, ROVEE-COLLIER
AND GARGANO
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