Hard faeces reingestion and the passage and recycling of large food particles

in the Japanese hare (Lepus brachyurus)

by H. HIRAKAWA ' and A. OKADA

' Forestry and Forest Products Research Institute Hitsujigaoka 7, Toyohira, Sapporo 062, Japan

Graduate School of Environmental Science, University of Tsukuba Ten-nodai 1-1 -1, Tsukuba, Ibaraki 305, Japan

Summary. - Upon finding the regular reingestion of hard faeces, we studied the passage and recycling of large particles in the diet of the Japanese hare (Lepus brachyurus) in relation to the timing of ingestion. Small, thin pieces of synthetic rubber, simulating large food particles, were mixed with commercial food pellets and subjected to voluntary intake during a short period of time at night, and their subsequent excretion in the faeces was recorded. Irrespective of time at intake, the markers were almost completely excreted by the end of the second night : when ingested early in the evening, most were excreted within that night, and as ingested later on, they were increasingly excreted on the second night. All hard and soft faeces excreted during the day- time resting period were reingested, and the markers, contained in both types of the daytime faeces, were thereby recycled. The results show that large particles in the diet are given another chance for digestion, through remastication and reingestion, when they are excreted during the daytime following ingestion. This suggests that hard-faeces reingestion does not result in mul- tiple recycling of poorly digestible large particles and leading to inefficiency in digestion.

Rbume'. - A I'occasion de recherches sur la reingestion des crottes dures, nous avons ktudik le passage et le recyclage des grosses particules dans le rCgime alimentaire du li5vre du Japon, Lepus brachyurus, en relation avec le moment de l'ingestion. De petits morceaux de caoutchouc synthCtique, simulant de grosses particules alimentaires, ont CtC mClangCs avec des granules de nourriture du commerce, soumis B une prise volontaire pendant une courte pCriode de la nuit, et on a enregistre l'heure de leur excrktion dans les feces. Quelle que soit l'heure de leur absorption, les marqueurs Ctaient presque complktement excrCtCs B la fin de la seconde nuit : quand ils atraient CtC ingkrCs t6t dans la soirCe, la plupart Ctaient excrCtCs dans la nuit meme, et quand ils avaient CtC ingCrCs plus tard, ils Ctaient excrktks en plus grand nombre au cours de la seconde nuit. Toutes les crottes, dures ou molles, excrCtCes pendant la pkriode de repos diurne, Ctaient rkingCrCes et les marqueurs, contenus dans ces deux types de crottes, Ctaient de ce fait recyclks. Les rksultats montrent que les grosses particules contenues dans le bol alimentaire ont ainsi une seconde chance d'etre digCrCes, par ltintermCdiaire de la remastication et de la rkingestion, quand elles sont excrCtCes pendant la journCe suivant leur ingestion. Ceci sugg5re que la rCingestion des crottes dures n'a pas pour rksultat un recyclage multiple des grosses particules difficiles B digCrer, induisant B une inefficacitk de la digestion.

Mammalia, t . 59, no 2, 1995 : 237-247.

MAMMALIA

INTRODUCTION

Leporids have long been known to produce two types of faeces, i.e., hard and soft, and to reingest soft faeces (Madsen 1939 ; Taylor 1939). However, Ebino et al. (1993) first reported the regular reingestion of hard faeces in Leporids for the domestic rabbit. Later, Hirakawa (1994) reported that the Japanese hare Lepus brachyurus reingests all hard and soft faeces during the daytime stay in the form : hard faeces are excreted and reingested within an hour after the hare enters a form early in the morning, and soft faeces are then excreted and reingested until the early afternoon, followed by hard faeces reingestion until the evening when the hare leaves the form. The faeces produ- ced during the night, when the hare forages, are hard faeces, which are discarded without being reingested.

Soft faeces are the excreta of the fermented caecum contents rich in vitamins and protein (Eden 1940 ; Kulwich et al. 1953 ; Huang et al. 1954), which are reingested so that the fermentative products can be digested and absorbed in the stomach and small intestine. Soft faeces reingestion (or caecotrophy) is thus an integral part of the diges- tive process in the Leporidae. Hard faeces are produced by a separation process at the proximal colon, which selectively diverts fluid and fine particles of digesta to the cae- cum (Bjornhag 1972 ; Pickard and Stevens 1972 ; Ruckebusch and Hornicke 1977 ; Ehrlein et al. 1983). Hence hard faeces are composed mostly of poorly digestible large particles.

Until the discovery of hard faeces reingestion, most of the large particles in the diet were considered to be discarded in hard faeces after one passage through the alimentary tract. However, this idea is no longer justified and the fate of large particles in the diet is expected to be variable : some are discarded, whereas others are reingested after the first passage ; some may be recycled more than once, if they are not broken down into fine particles by remastication. The fate of large diet particles should highly depend on the timing of the ingestion or reingestion in relation to the phase of daily activity.

Daily caecotrophy rhythm has been known in the domestic rabbit and some other Leporidae species, but few passage time studies in the past (conducted mostly for the domestic rabbit) have scrutinized the temporal dynamics of the passage and recycling of diet particles. Hard faeces reingestion and its possible effects on the excretion of large particles have naturally been totally neglected. In this paper, we report how large particles in the diet of the Japanese hare are passed, recycled, and eventually discarded in relation to the timing of ingestion.

MATERIALS AND METHODS

Hares

Three well-tamed adult hares were used in turn. These were kept in a room (3.6 m X 3.6 m) with natural light condition in the daytime but with dim red light during the night. Their feeding activities were continuously monitored throughout the experiments by measuring the weight of the feeder on an electric balance connected to a portable computer. All the hares showed a normal daily activity rhythm during the experiments : they fed during the night and rested during the day. The hares were fed as usual with commercial food pellets during the experiments (Table 1).

General experiment procedure Thin pieces of synthetic rubber (thickness : 0.2 mm, size : 1 mm X 1 mm or 1 mm

X 2 mm) in five colors were used to simulate large particles in the diet. These were mixed with a paste of water and commercial food pellets, which was then dried and

PASSAGE OF LARGE PARTICLES IN THE HARE 239

TABLE 1. - Ingredients and chemical composition of the commercial food pellets used in the experiments.

Ingredients ( % )

Fish & Soybean meal 10.0

Lucern meal 38.0

Wheat flower & bran; maize 49.8

Minerals and vitamins 2.2

Chemical composition (%)

Water 8.5

Crude protein 21.2

Crude fat 3.5

Crude fiber 11.4

Minerals 8.1

again made into pellets. The pellets with markers were placed in the feeder for some period of time during a night as a replacement for normal pellets and left to voluntary intake by the hares.

During the first three nights, the hares were monitored with a video system and faeces were collected every time they were excreted. The faeces excreted in the fourth and fifth nights were collected once daily in the following morning. The markers were recovered from the faeces by watering and mashing faeces and manually picking up each piece. Both intact and fragmented pieces were counted, but fragmented pieces smaller than half of the original size were neglected to avoid double counting. In the later experiments, the markers in the pellets left uneaten in the feeder were counted to see how many pieces were actually ingested.

Experiments for marker excretion by natural defecation Experiments were conducted five times with minor variations in timing and dura-

tion of exposing marker pellets for voluntary intake of hares. In trial 1, marker pellets of one color were given from 18:OO to 20:OO and in trial 2, marker pellets of four colors were each given for 1.5 hours starting at 18:00, 19:30, 21:00, and 22:30. In trials 3 and 4, marker pellets of five colors were substituted in turn for normal pellets every 2.5 or 2.0 hours from the evening to the morning, and after one feeding bout, which lasted only several minutes, they were again replaced back with normal pellets so that intake for each colored marker was restricted to a short period of time. Trial 5 was as trial 3 and 4, except that marker pellets of each color were placed every 1 hour from midnight until morning. Markers of 1 mm X 2 mm were used for trials 1 and 2, and 1 mm X 1 mm for trials 3 , 4 and 5.

Experiment for marker excretion in daytime faeces To estimate the number of large particles excreted and reingested during the day-

time resting period, we fed marker pellets of five colors to one hare at 2.5 hour inter- vals during a night in the way as described above, and then attached the hare with a reingestion-preventing collar when it entered the resting phase in the morning. Thus we collected hard and soft faeces excreted, which would otherwise be reingested.

Statistics and calculation

MAMMALIA

Three types of passage time were calculated : the minimum passage time was the time that has elapsed between the time at intake (the start time of feeding marker pel- lets) and the first appearance of the marker in the faeces ; 98 % excretion time was the time that elapsed since the time at intake until 98 % of the recovered markers were excreted ; mean retention time (MRT) was calculated as MRT = Cpiti, where pi was the proportion of markers to the total recovered and ti was the time that elapsed between ingestion and excretion (Blaxter et al. 1956).

G-test was used for the comparisons of recovery and fragmentation rates of the markers (Sokal and Rohlf 1973). Mann-Whitney's u-test was used for the comparisons of passage time among trials.

RESULTS

General pattern of daily activity

During the experiments (trials 3, 4, and 5), the hares on the average started fee- ding at 17:Ol (n= 15, 16:15 - 1753) andended it at 4:26 (n= 14, 3:18 - 5:18). Defeca- tion started at 17:34 (n = 15, 16:29 - 18:30) and ended at 04:43 (n = 15, 358 - 5:28). Reingestion activities in the daytime were not always monitored throughout the experi- ments, but the available data showed that the pattern of the reingestion of soft and hard faeces was as usual (Fig. 1).

Time of Day ternpora;ily active

Fig. 1 . - A typical daily activity pattern observed during the experiments. The increasing and decreasing lines represent defecation and feeding processes, respectively. Solid and open circles indicate the time of reingestion of hard and soft faeces, respectively. The schemata above illustrate the digesta flows at different phases of foraging during the night, and hard and soft faeces reingestion during the daytime.

PASSAGE OF LARGE PARTICLES IN THE HARE 24 1

Recovery rate

The recovery rate of markers (total no. of pieces recovered vs. ingested no.) was significantly higher in trial 5 than trials 3 and 4 (G-test, p <0.01), but there was no significant difference within each trial except for a low recovery rate of white markers (G-test, p < 0.01) in trial 4 for unknown reason (Table 2). No consistent differences in recovery rates among colors were detected.

Excretion process

Of all the marker pieces recovered by the end of the fifth night (5764), 99.6 % was excreted by the end of the second night and 0.4 % was excreted on the third night. Only one piece (0.02 %) was recovered on the fourth and none on the fifth night. The time at intake of the markers strongly affected the excretion rate of the first night but not that of later nights (Table 2, Fig. 2). The markers ingested early in the evening

m : first night : second night

Time of Day at Marker Intake

Fig. 2. - Time at marker intake and excretion rate at the end of the first and second nights. The results of all the trials are presented.

were mostly excreted within that night, but those ingested later on were increasingly excreted on the second night (Fig. 3). : In trials 3, 4, and 5, the minimum passage time was very short ; the shortest

record was 2:00 h and longest was 3:22 h (n = 13, 2:36 + 0:25 h), excluding two extreme cases, in which markers were ingested after 3:30 and first found in the faeces excreted on the second night, 13 to 14 hours after ingestion (Fig. 4). Peak density in the faeces came 3 to 5 hours after ingestion within the night, or 13 to 16 hours later on the second night. The time for excretion of 98 % of the markers was 23:31 + 1:04 h (n = 14, 20: 19 - 25:03) excluding one extreme case of 10:04 h.

In trial 2, the minimum passage time, 4:25 h on average (n = 3:59 - 5:01), was significantly longer than that in trials 3, 4, and 5 (Mann-Whitney test ; p < 0.01), but the 98 % excretion time, 22:13 h on average (n = 4, 21.04 - 23:37) was not signifi- cantly different (Mann-Whitney test ; p > 0.05).

MAMMALIA

h

A

12 1 8 00 06 12 18 00 06 12 18 00 06 12

Time of Day

Fig. 3. - The excretion process of markers ingested at different times during the night in trial 4. The uppermost graph shows the defecation process. In the lower graphs, the arrows indicate the time when pellets with markers were ingested ; the solid lines indicate the cumulative excretion of markers as percent of the total recovered ; the solid squares indicate the marker density in faeces.

Mean retention time was increased as the time at intake was becoming later in the night. The longest of mean retention time of 16:29 h was more than three times as long as the shortest of 4 5 1 h (Fig. 4).

Fragmentation of markers

Of pieces measuring 1 mm X 1 mm (trials 3, 4, and 5), 2.8 % recovered in the first night and 7.5 % in the second night were fragmented, with an average fragmenta-

PASSAGE OF LARGE PARTICLES IN THE HARE

0 x 0 : trial 2 *+. : trials 3,4 and 5 g: first excretion $: mean retention time 8: 98% ecxretion

Time of Day at Marker Intake

Fig. 4. - Minimum passage time (OO), 98 % excretion time (mu) and mean retention time (MRT = &piti, +x) of markers vs. time at marker intake. Symbols OOX are for trial 2, and Om+ for trials 3, 4 and 5.

tion rate of 5.2 % of the total recovered (Table 2). Of pieces measuring 1 X 2 mm (trial 2), 18.5 % recovered in the first and 42.6 % in the second night were fragmented, with an average of 23.7 % of the total recovered. The differences in fragmentation rates bet- ween the first and second nights were significant for both sizes of pieces (G-test, p < 0.01). The fragmentation rate was significantly greater for the pieces of 1 mm X 2 mm than for those of 1 mm X 1 mm (G-test, p < 0.01).

Markers in daytime faeces

In the reingestion-prevention experiment, the hare entered the resting phase earlier than usual for unknown reason and after being collared at 3:20 it showed highly stres- sed behavior. The hare was scared of the observer and its faeces excretion schedule was delayed ; excretion of soft faeces began at 7:34 and hard faeces at 19:57, soon after which we stopped the experiment to avoid overstressing the hare. The same indi- vidual began reingestion of hard faeces at 12:29 on average (n = 8) during earlier expe- riments, which is normal. Because of this, we could not sample all the daytime hard and soft faeces. As a result, we could not obtain data on the number of markers that are recycled through reingestion. A notable result, however, was that soft as well as hard faeces contained the particle markers, although the number of pieces per dry weight of faeces was much lower in soft than in hard faeces (34 pieceslg in soft faeces vs. 71 and 60 pieceslg in hard faeces excreted before and after the excretion of soft faeces, respec- tively).

MAMMALIA

DISCUSSION

The temporal pattern of marker excretion (Table 2) suggests that recovery loss cannot be accounted for by the delayed excretion after the fifth night. Fragmentation of marker pieces is probably the major cause of the recovery loss. First, recovered frag- ments that were smaller than half of the original size were not counted. Second, some markers must have been broken down to pieces too small to detect ; some may have been rendered small enough to behave as fine particles and may have actually been excreted later. The increase in the fragmentation rate of the marker pieces from the first to the second night is probably due to the effect of remastication which accompanied reingestion. This suggests that recovery rate might be more underestimated in the second, or later nights. Hence, we need to qualify our results in that nearly all the mar- kers were excreted within the first two nights as far as they remained large.

TABLE 2. - Time at intake and recovery of markers in the faeces.

marker time at minites no. no. pieces recwered at night recov. no. fragmented pieces trials color intake intake intake 1st 2nd 3rd 4-5th total rate% 1st 2nd 3rd-

trial 1 yellow 18:Ol - 741 191 14 0 946 - - -

trial 2 white 18:09 70 - 696 62 1 0 759 - 112 21 1 orange 1953 48 - 398 37 1 0 436 - 97 21 1 green 21:22 60 - 703 219 2 0 924 - 110 80 2 black 22:37 77 - 329 241 3 0 573 - 75 116 2 subtotal 2126 559 7 0 2692 394 238 6

trial 3

trial 4

trial 5

white 18:14 5 196 191 0 0 0 191 97.4 3 0 0 orange 20:26 6 210 186 7 0 0 193 91.9 5 0 0 yellow 22:30 5 167 138 17 0 0 155 92.8 7 1 0 green 00:14 1 33 23 7 0 0 30 90.9 1 0 0 black 02:08 2 101 23 70 1 0 94 93.1 1 10 1 subtotal 707 561 101 1 0 663 93.8 17 11 1

white 17:38 5 178 133 17 0 0 150 84.3 1 2 0 orange 20:27 2 71 55 15 0 0 70 98.6 4 1 0 yellow 22:34 4 179 105 68 0 0 173 96.6 4 6 0 green 01~06 8 162 11 146 0 0 157 96.9 0 14 0 Mack 03:41 5 200 0 190 0 0 190 95.0 0 22 0 subtotal 790 304 436 0 0 740 93.7 9 45 0

white 00:15 6 171 114 55 0 0 169 98.8 2 2 0 orange 01:08 3 65 30 32 0 1 63 96.9 0 0 0 yellow 02:21 3 138 23 11 1 1 0 135 97.8 1 7 0 green 03:28 7 236 8 220 2 0 230 97.5 0 11 0 black 0404 3 128 0 126 0 0 126 98.4 0 5 0 subtotal 738 175 544 3 1 723 98.0 3 25 0

subtotal for trials 3.4 and 5 2235 1040 1081 4 1 2 1 2 6 95.1 29 81 1

TOTAL 3907 1831 25 1 5 7 6 4

Time at intake indicates the starting time of feeding marker pellets. * In trials 1 and 2, l x 2 nun markers were used and marker pellets of each color were placed for 2 and 1 .5 h, respectively.

In trials 3.4 and 5, 1 x 1 mm markers were used and marker pellets of each collor were placed at every 2.0,2.5, and 1.0 h interval, respectively, which were replaced back with normal pellets after one feeding bout.

PASSAGE OF LARGE PARTICLES IN THE HARE 245

The separation at the proximal colon is a size-dependent mechanical process ; the threshold is likely in the range of 0.1 mm to 0.3 mm (Bjornhag 1972). The size of the markers used in this study was thus big enough to simulate the movement of large par- ticles in the process. However, Pickard and Stevens (1972) reported that about 17 % of 2 mm X 2 mm (or 60 % of 2 mm X 5 mm) plastic tube markers were retained in the stomach for more than 24 hours. This indicates that the stomach selectively holds large food crumbs, which may account for the retention of intact soft faecal pellets in the stomach of the rabbit for more than six hours (Griffiths and Davies 1963). Some of the remarkably longer passage times of solid markers recorded in the past seem to be rela- ted to this effect (e.g., Bailey 1968 ; Clemens and Stevens 1980). In contrast, the short passage time in trials 3, 4 and 5 indicates that the markers were not much affected by such a selective retention for large crumbs in the stomach. The significantly longer minimum passage time in trial 2 than that in trial 3, 4 and 5 might be related to this effects. The maximum size of large particles found in the normal hard faeces of the Japanese hare was 1 to 2 mm in length - not much different from the markers we used.

In the separation process at the proximal colon, the retrograde movement of haus- ' tra selectively extracts and carries back fluid and fine particles from the digesta, which is being carried forward (Ehrlein et al. 1983). It should not be possible that some large particles are accidentally dragged back to the caecum by this process. It may thus seem puzzling that marker pieces were excreted in soft faeces as well as in hard faeces. However, this is explained by the fact that when the separation process is operating at the proximal colon, digesta flows from the ileum into the caecum and mixes with cae- cum contents before entering the proximal colon (Bjornhag 1972 ; Pickard and Stevens 1972 ; Ehrlein et al. 1983) ; hence the caecum contents are never free from large par- ticles. Further, the flow of digesta from the stomach to the caecum seems not to be sus- pended even when caecum contents flow out to produce soft faeces : Gidenne (1987) showed that fresh food in the stomach decreased rapidly during the morning when cae- cotrophy was practiced and Bouyssou et al. (1986) showed that the stomach-ileum flow of markers did not vary with the timing of marker injection during a day.

Without being interrupted by reingestion phase, the minimum passage time of large particles was as short as 2 hours and even 98 % excretion time was as short as 10 hours. However, the times increase by more than 10 hours if the reingestion phase, which lasts for half a day in the daytime, cuts into this process. This indicates that the passage of large particles through the alimentary tract is very fast, but their retention in the alimentary tract can be prolonged because of the delay in excretion by recycling during the daytime. This results in the increasingly longer mean retention time as time at intake is becoming later (Fig. 4). This implys that there is no single representative in mean retention time in Leporidae, and that the presentation of mean retention time could be misleading if the time at intake is not specified.

Although caecotrophy in Leporids has been known for decades, the effects of time at intake (or at injection) on the excretion of markers have not been well investigated in the past. In some passage rate studies in the past, the time of marker injection was given, but very often it was not related to the phase of daily activity.

If rabbits are kept under a constant photoperiod regime (for example, 12 h light : 12 h dark) and food is given ad lib., then we can possibly assume that rabbits practice caecotrophy (soft faeces reingestion) in the early half of the light phase (Jilge 1974, 1976 ; Hornicke and Batch 1977). However, even if this is the case, the second caeco- trophy phase might occur around the midnight in some rabbits (Jilge 1982). Further, nighttime hard faeces are reingested in the Japanese hare if food is given less than requirement and hence depleted during the night (Hirakawa 1994) and the same might

246 MAMMALIA

happen in the domestic rabbit. This indicates the importance of confirming the rhythm of feeding and reingestion under experimental conditions.

This study showed that large particles in the diet of the Japanese hare were almost completely discarded by the end of the second night even when recycled through hard faeces reingestion. This was resulted from the remarkably fast passage of large par- ticles through the alimentary tract (recall that large particles ingested early in the eve- ning were almost completely discarded within that night, then it is expected that recy- cled particles, as reingested during the daytime, are completely discarded in the following night).

An almost complete evacuation of large particles by the end of the second night indicates that there is no such disadvantage to hard faeces reingestion in that some poorly digestible materials recycle many times in vain, leading to inefficiency in diges- tion. Large particles are given another chance for digestion, through remastication and reingestion, when they are excreted during the daytime following ingestion.

The reingestion of hard faeces is equivalent to rumination in foregut fermenters in the sense that it is practiced during the resting phase and that poorly digestible large particles are remasticated. Thus it may well be called << pseudo-rumination >>, a term proposed by Taylor (1940) for soft faeces reingestion but not adopted by subsequent authors as inappropriate.

ACKNOWLEDGEMENTS

We thank Ms. Barbara Andre for correcting English of the manuscript.

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