J. Anim. Physiol. a. Anim. Nutr. 59 (1988), 160-166 0 1988 Verlag Paul Parey, Hamburg und Berlin ISSN 0044-3565

Receipt of Ms. 4. 9. 1987

Institut fur Veterinar-Physiologie der Universitat Zurich und I Fakultatsstelle f i r Biometrie der Veterinarmedizinischen Fakultat der Universitat Zirich

Free-feeding pattern of pygmy goats eating a pelleted diet

W. LANGHANS, M. SENN, E. SCHARRER and E. EGGENBERGER’

Introduction

Feeding in man and animals occurs in clusters of feeding bouts (= meals), separated by periods of non-feeding (intermeal intervals = IMIs). The frequency and circadian distribu- tion of meals vary considerably between species (AUFFRAY and MARCILLOUX 1980, 1983; HIRSCH 1973; LE MAGNEN and TALLON 1963; METZ 1975; RASHOTTE et al. 1984; SANDERSON and VANDERWEELE 1975). Under ad libitum feeding conditions, a significant positive corre- lation between meal size and duration of the subsequent IMI (post-meal IMI) has often been observed in the rat (BERNSTEIN 1975; DAVIES 1977; DE CASTRO 1975; LE MAGNEN and DEVON 1984; LE MAGNEN and TALLON 1963, 1966; ROSENWASSER et al. 1981; THOMAS and MAYER 1978) and also in some other species (AUFFRAY and MARCILLOUX 1983; HANSEN et al. 1981; RASHOTTE et al. 1984; SANDERSON and VANDERWEELE 1985). This post-meal correla- tion indicates that food intake is regulated from meal to meal, with a meal-related post- prandial factor contributing to the maintenance of post-prandial satiety (LE MAGNEN and DEVOS 1984; LE MAGNEN and TALLON 1963). Analysis offeeding patterns may thus help to understand the mechanism of food intake regulation. In contrast to the profound know- ledge about the feeding behavior of the laboratory rat, little is known about the feeding patterns of ad libitum fed ruminants (BAILE 1979; CHASE et al. 1976; METZ 1975; WANGS- NESS et al. 1976). The meal pattern of goats, for instance, although sometimes recorded (BAILE 1971; DE JONG et al. 1981), has not been described in detail yet. In the present study we therefore recorded and analyzed the feeding behavior of freely-feeding pygmy goats.

Animals and housing conditions: Eight adult, female, non-lactating, and non-pregnant pyg- my goats, weighing 20-33 kg, were used. The goats were individually housed on wood shav- ings in pens (1.25 x 1.35 m), located in a room, which was kept on an artificial dark-light cycle of 12 h each with the lights o n at 9.00. The room temperature was 20 f 2°C. The goats were fed ad libitum a “complete” pelleted diet (Hypona-Optimal 888, Volg Winterthur). The chemical composition and feeding value of the diet was as folows: Dry matter: 86.2%, in dry matter: 16.9% crude protein, 12.8% crude fiber, 7.9% ash, and 5.0 MJ net energy for lactation per kg (values given by the manufacturer). Tap water was always available. Before the experiment, the goats were adapted to diet and maintenance conditions for several months. Data acquzsition: The goats were forced to feed out of spill-resistant food containers, which were fixed on scales (Mettler PE 6). Scales and food containers were sheltered by a wooden box with a hole on the front side. The hole was big enough to allow unhindered access to food (Fig. 1). The actual weight of the food containers ( f 1 g) was checked each minute automatically by a Hewlett Packard personal computer (HP 85 B). The computer was pro-

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Freegeeding pattern of pygmy goats 161

I I

-Wooden b o x -

Front hole -

-Food container-

- Scale -

I - F l o o r ~ --

Side - view Front - view

Fig. 1. Side-view (left) and front-view (right) of a feeding unit.

grammed to recognize when the pattern of food removals fits the preset meal definition and to print out the time of meal onset, the time of meal end, the size (g) and duration (min) of the meal, and the time passed since the end of the preceding meal, i. e. the inter- meal interval (IMI). Meals were defined as food removals exceeding 5 g, separated by at least 15 min of non-feeding. With this meal definition, the recorded meals accounted for almost 95% o f the cumulative food intake, which was recorded every second hour and printed out after 12 and 24 h of data collection. Meal patterns were recorded over 4 weeks, for 6 days each week. O n the 7th day, the food containers were refilled, the room was cleaned, and the goats’ body weight was measured. Data analysis: All meal parameters were at first computed for each goat separately. Similar- ly, correlation coefficients were computed on raw data, i.e. on all individual meals, for each goat separately. The tables show the means of the 8 individual values. The significance of differences between bright and dark phase was tested with the Wilcoxon matched pair signed rank test. P values less than 5% were considered significant.

Table 1. Meal parameters and cumulative food intake o f pygmy goats fed a pelleted diet

24 h Light Dark ~~

Meal frequency Meal size (9) Meal duration (min) Duration of IMI (min) Satiety ratio’ Cumulative food intake (9)

- 12 f 0.7 8 * 0.9 4 * 0.3‘ 49 f 4 43 * 4 62 * 5’ 24 f 4 22 * 3 28 * 7 87 f 6 63 f 6 170 * l 3 ’

610 f 2 1 384 f 14 226 * I S ’ 2.6* 0.2 2.0* 0.2 4 . 0 k 0.3’

Values are means f SEM of the 8 goats’ individual values. I Significantly (p <0.05) different from “Light”. ’ Duration of post-meal IMVmeal size.

162 W. Langhans, M. Senn, E. Scharrcr and E. Eggenberger

Table 2. Corre la t ions between meal parameters

Correlation coefficient (r) 24 h Light Dark

Meal size vs. meal duration 0.476 * 0.078 (8) 0.484 * 0.074 (8) 0.521 * 0.089 (7) Pre-meal IMI vs. meal size 0.084 f 0.0402 (0) Meal size vs. post-meal IMI’ 0.350f0.033 (8) 0.171 f0.044 (2) 0.377*0.051’(7)

Values are means f SEM o f the 8 goats’ individual correlation coefficients. Number of animals showing significant (p < 0.05) correlation is given in parentheses. ’ Partial correlation coefficients (Sachs, 1984) are given t o correct for the influence o f pre-meal

’ Significantly (p < 0.05; Wilcoxon matched pair signed rank test) different from “Light”.

0.121 f 0.045 (2 ) 0.273 5 0.048 (7)

interval on meal size.

Results

Over 24 days, 2304 meals were recorded for all goats. Individual animals ate between 227 and 366 meals. O n an average day, 8 meals corresponding to about 63% of total 24 h food intake, were eaten during the bright phase (= light) and 4 meals during the dark phase (= dark) (Table 1). Meal size was smaller and IMI was shorter during light than during dark (Table 1). The satiety ratio (= duration of post-meal IMI/meal size) was higher during dark than during light (Table 1). The respective values were calculated for individual meals and are not identical with the quotients of mean IMI durations and mean meal sizes listed in Table 1, because meal sizes showed some deviation from the normal distribution (values < X prevailed) and varied relatively more than IMI durations, especially during dark.

The cumulative food intake data shown in Table 1 include the nibbling bouts between meals. Note, however, that only 34 g per 24 h could not be attributed to the recorded meals. The goats’ body weight did not change during the experiment. When all diurnal and nocturnal meals were considered, meal size was positively correlated to meal duration and duration of post-meal IMI in all goats (Table 2). Meal size and duration of pre-meal IMI were correlated in only 2 goats (Table 2). When diurnal and nocturnal meals were consi- dered separately, meal size was positively correlated with duration of post-meal IMI during dark (significant in 7 animals, Table 2). During light, meal size was rather correlated to duration of pre-meal IMI (significant in 7 animals, Table 2). The correlation between meal size and meal duration was similar during light and dark (Table 2). The circadian distribu- tion of meals and the circadian variations of meal size and duration of IMI are shown in Fig. 2 and 3, where the actual time of meal end is plotted against meal size (Fig. 2) or dura- tion of post-meal IMI (Fig. 3) for all 2304 individuals meals. Both parameters remained fairly constant during light (Fig. 2 and 3). With dark onset, however, meal size sharply increased (Fig. 2). The size of later nocturnal meals was roughly within the range observed for the size of diurnal meals. However, there were apparently less small meals (meal size <50 g) during dark than during light (Fig. 2). The duration of post-meal IMIs also increased around dark onset. Longer IMIs than during light occurred until about 4.00. Only a few nocturnal IMIs lasted less than 100 min (Fig. 3). Further, it is noteworthy that meals were evenly distributed over the bright phase (Fig. 2). During dark, only a few meals occurred between 22.00 and 24.00 (Fig. 3). No clear circadian evolution of the post-meal or pre-meal correlation was found (not shown).

Free-feeding pattern of pygmy goats 163

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Fig. 2. Circadian distribution of meals and circadian variations in meal size. See text for further details.

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164 W Lungbans, M. Senn, E. Scbarrcr and E. Egenberger

Discussion

The pygmy goats, fed a pelleted diet ad lib., ate 12 meals of about 49 g (= 21 1 kJ net energy lactation) per 24 h. A similar meal frequency (10-12 meals/day) has been reported for goats (BAILE 1971) and steers (CHASE et a]. 1976), while only 6 (BAILE 1979) or 8 (WANGSNESS et al. 1976) meals per day have been observed in freely feeding sheep.

Direct comparison ofour data with these studies of feeding behavior in other ruminants is difficult, however, because other techniques for meal pattern recording (BAILE 1971, 1979; WANGSNESS et al. 1976) and other meal definitions (BAILE 1971; WANGSNESS et al. 1976) were used. Many other species (cat, horse, rhesus monkey, rat) eat 8-10 meals per day (HANSEN et al. 1981; KANAREK 1975, LE MAGNEN and TALLON 1963,1966; RALSTON 1984). A lower meal frequency has been reported for dogs (6 meals per day (RASHOTTE et al. 1984)) and pigs (3 meals per day (AUFFRAY and MARCILLOUX 1980, 1983)), while guinea pigs and rabbits eat up to 30 meals per day (HIRSCH 1973; SANDERSON and VANDERWEELE 1975).

The pygmy goats showed a distinct circadian rhythm in feeding behavior. They ate clearly more during the bright phase (= light) than during the dark phase (= dark). This is consistent with the feeding behavior of grazing sheep and cattle (LOFGREEN 1957) or of ste- ers fed mixed rations (CHASE et al. 1976). During dark, meal frequency was lower, but meal size was greater (at least at dark onset) than during light. This is interesting, because in rats, which eat primarily during dark, a low meal frequency and smaller meals contribute to the low food intake during light (LE MAGNEN 1983; LE MAGNEN and TALLON, 1963, 1966; ROSENWASSER et al. 1981). In pigs, the low nocturnal food intake is due to less meals of about the same size as during light (AUFFRAY and MACRILLOUX 1983). The higher satiety ratio of nocturnal compared to diurnal meals indicates that a given amount offood is more satiating during dark. This may reflect an increase in mobilization of body fat in ruminants during the night. A nocturnal increase in plasma non-esterified fatty acid levels has in fact been reported for lactating cows (BLUM et al. 1985). An enhanced nocturnal lipolysis may contribute to the low nocturnal food intake of ruminants, because intravenous infusions of fatty acids decreased food intake in sheep (VANDERMEERSCHEN-DOIZ~~ and PAQUAY 1984). A causal relationship between enhanced lipolysis and low food intake during light has been postulated for rats (LE MAGNEN 1983).

The peak in meal size after dark onset is hard to explain. It is especially puzzling, because the respective pre-meal IMI was not generally longer than diurnal IMIs. Interest- ingly, in the only other report of circadian variations of meal parameters for ruminants (cattle), meal size peaked in the evening, just before darkness (METZ 1975). Significant posi- tive correlations between meal size and duration of post-meal IMIs (post-meal correla- tions) have been reported for rats (BERNSTEIN 1975; DAVIES 1977; DE CASTRO 1986; LE MAGNEN and DEVOS 1984; LE MAGNEN and TALLON 1963, 1966; ROSENWASSER et al. 1981; THOMAS and MAYER 1978) dogs (RASHOTTE et al. 1984), pigs (AUFFRAY and MARCILLOUX 1983), rabbits (SANDERSON and VANDERWEELE 1975) and rhesus monkeys (HANSEN et al. 1981). The present results add the pygmygoat to this list. The observed correlation coeffi- cients are within the range reported for other species (AUFFRAY and MARCILLOUX 1983; HANSEN et al. 1981; RASHOTTE et al. 1984; SANDERSON and VANDERWEELE 1975) and for the rat, when short IMI definitions were used (DE CASTRO 1975; ROSENWASSER et al. 1981; THOMAS and MAYER 1978) and when correlations were computed on raw data (BERNSTEIN 1975; DE CASTRO 1975; ROSENWASSER et al. 1981; THOMAS and MAYER 1978). The fact that these correlations are rather small is not surprising, given the complexity of food intake regulation in general (LANGHANS and SCHARRER 1987; LE MAGNEN 1983; SCHARRER 1984; WEINGARTEN 1985). There is only one other report of a significant post-meal correlation for ruminants (sheep), eating a roughage diet (BAILE 1979). These calculations were, however, performed with pooled data instead of raw data, i.e. meal sizes were rank ordered into 10 groups ranging from the 10% smallest meals to the 10% largest. Accordingly, the inter-

Free-/eeding pattern of pygmy goats 165

vals fell also into 10 groups, and correlation coefficients were calculated from the group means (BAILE 1979). This procedure has been shown to lead to statistical bias (PANKSEPP 1973). Pooling of our data, for instance, yields post-meal correlation coefficients of about 0.8. In the present experiment, the post-meal correlation was stronger during dark than during light. A similar circadian variation of the post-meal correlation has been reported for rats (LE MAGNEN and DEVOS 1984; LE MAGNEN and TALLON 1963, 1966). These and our findings cannot be compared directly, however, because unlike pygmy goats, rats are hyperphagic at night (LE MAGNEN 1983; LE MAGNEN and TALLON 1963,1966). During light, meal size was positively correlated to duration of pre-meal IMI rather than to duration of post-meal IMI. This is in line with previous observations o f a pre-meal correlation in cattle (METZ 1985) and sheep (BAILE 1979), eating a roughage diet. In these studies, however, noc- turnal and diurnal meals were not analyzed separately (BAILE 1979; METZ 1975). A pre-meal correlation has also been observed in humans (DE CASTRO 1986) where it may be due to the common schedule of 3 to 5 fixed meals per day (DE CASTRO 1986). In laboratory animals a pre-meal correlation is only found, when the animals are food deprived (LEVITSKY 1970) or kept on a meal feeding schedule (LEVITSKY 1974). The circadian variations ofpost- and pre- meal correlations, observed in the present study, suggest that during dark and light food intake of freely feeding pygmy goats is regulated differently. During dark, when the size o f a meal influences the duration of the post-meal IMI, pygmy goats apparently begin a meal partly in response to the cessation of a postprandial satiety factor, which is maintained in relation to the size of the previous meal. In contrast, during light, meal initiation seems to be fairly independent of the internal state of nutrient depletion. In this case, meal initia- tion may be conditioned (DE CASTRO 1986; WEINGARTEN 1985). Once a meal is initiated, however, pygmy goats partly eat until a deficit has been corrected which is proportional to the duration of the pre-meal IMI. Therefore, the matching of food intake to energy require- ments seems to be accomplished primarily through variations in IMI duration during dark and through variations in meal size during light. There is evidence that meal frequency and meal size are primarily regulated by metabolic and gastrointestinal feedback-signals, respectively (LANGHANS and SCHARRER 1987; LE MAGNEN 1983; SCHARRER 1984). The pres- ent results therefore suggest that in pygmy goats, metabolic feedback-signals controlling food intake prevail during dark, and gastrointestinal signals during light.

To summarize, the results demonstrate that feeding behavior of pygmy goats follows a distinct circadian cycle and suggest that food intake in ruminants is regulated from meal to meal, with different factors prevailing during light and dark.

Abstract

The meal pattern of ad libitum fed pygmy goats was recorded and analyzed (12 h light/l2 h dark). Pygmy goats, adapted to a complete pelleted diet, consumed 12 meals per day. Eight meals, corresponding to about 63% oftotal daily food intake, occurred during the bright phase and 4 meals during the dark phase of the lighting cycle. Mean meal size was greater during the dark phase than during the bright phase. Meal size was positively correlated with the duration of the post-meal interval during the dark phase and with the duration of the pre-meal interval dur- ing the bright phase. The results demonstrate that food intake in pygmy goats follows a distinct circadian cycle. Further, food intake of pygmy goats is apparently regulated from meal to meal, with different factors prevailing during light and dark.

Zusammenfassung

Verzehrsmuster von Zwergziegen bei ad-libitum Fti'tterung e k e s pelletierten Alleinfutters

Das Verzehrsmuster von ad libitum gefutterten Zwergziegen wurde kontinuierlich registriert und analysiert. Die an ein pelletiertes Alleinfutter adaptierten Tiere frai3en durchschnittlich 12 Mahlzeiten pro Tag (12 h Hell412 h Dunkelphase). Davon entfielen 8 Mahlzeiten, entspre- chend ca. 63% der gesamten taglichen Futteraufnahme, auf die Hellphase und 4 Mahlzeiten auf

166 W. Langhans, M. Senn, E. Scharrcr and E. Eggcnbergcr

die Dunkelphase. I m Mittel waren die Mahlzeiten in der Dunkelphase groRer als in der Hell- phase. Wahrend der Dunkelphase war die MahlzeitengroRe mit der Dauer des jeweils folgen- den, wahrend der Hellphase mit der Dauer des jeweils vorangehenden Mahlzeitenintervalls positiv korreliert. Die Ergebnisse zeigen eine deutliche circadiane Rhythmik des Verzehrsver- haltens von Zwergziegen. Ferner wird die Futteraufnahme von Zwergziegen anscheinend von Mahlzeit zu Mahlzeit reguliert, wobei wahrend der Hell- und Dunkelphase unterschiedliche Faktoren von Bedeutung sind.

Acknowledgement

We thank Ms. C . GROIER and Mr. T. SYDLER for their help.

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Adresse der Autoren: Institut fur Veterinar-Physiologie der Universitat Zurich und Fakultats- stelle fur Biornetrie der Veterinarmedizinischen Fakultat der Universitat Zurich, WinterthurerstraRe 260, CH-8057 Zurich, Schweiz

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