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The role of the crop in the feeding behaviour of the domestic chicken
Anim . Behav., 1970, 18, 6 3 3 -639
THE ROLE OF THE CROP IN THE FEEDING BEHAVIOUR OF THE DOMESTIC CHICKEN BY A. J . RICHARDSON A.R .C., Poultry Research Centre, King's Buildings, West Mains Road, Edinburgh 9
Although the mechanisms controlling the food intake of mammals have been extensively investigated, there has been very little comparable work on avian species . There are gross anatomical differences between the digestive tracts of mammals and birds, and also differences in metabolism, for example the reaction to insulin (Evans 1969), which suggest that there may be differences in the regulation of feeding behaviour . The experiments reported here are part of a series on various aspects of the system that controls feeding in the chicken . It is planned to include oral factors, distention mechanisms in the gut, biochemical and nutritional factors and the integration of all these in the central nervous system . The present paper is concerned solely with the part played by the crop . The size and shape of the crop varies widely between species . Farner (1960) states that it is unlikely that all the structures designated as crops are homologous . If this is so, then it is also unlikely that the part played by the crop in the control of food intake will be the same in all species. However, since it is derived in all species from the same general part of the oesophagus, which is homologous, then the basic physiology and pharmacology will probably be similar . Surgical Removal of the Crop Experiments by von Ihnen (1928) showed that presence of the crop is not necessary for the domestic chicken's survival . Later, Fisher & Weiss (1956) found that removal of the crop from 1-week-old chicks had no effect upon their subsequent weight-gain or food intake when food was continuously available . However, if feeding was restricted to two 1-hr periods per day, cropectomized birds made lower weight gains than normal controls (Feigenbaum, Fisher & Weiss 1962) . Experiment 1 Methods . This experiment was undertaken to check the findings on the effect of crop removal mentioned above . The crop was removed from ten male leghorn chicks at 1 to 2 weeks of age, by the procedure described in Fisher & Weiss
(1956) . In another ten chicks the crop was made ready for excision in the same way and the skin wound closed, leaving the crop intact . At 10 weeks the food intake of the two groups was measured under conditions of 24, 2, 11, 1 and f hr access to food per day . Data were collected over 4 days for continuous access to food and 2 days for each of the restricted-feeding periods . The data for all unrestricted and all restricted periods were averaged for each bird and the two groups compared by t-test . The rearing and housing of the birds was the same in this and subsequent experiments . They were kept in groups from hatching till 12 weeks of age and were then rehoused into single standard battery cages 28 x 40 x 45 cm. The food containers were 12 . 5 x 15 x 10 cm and spillage was very slight. All birds could see and hear other birds in the battery, which was lighted from 07 .00 to 21 .00 hours. Water was available at all times . The diet used was pelleted and had a metabolizable energy value of 2800 kcal per kg . Results. The cropectomized birds had a lower average body weight than the controls for 1 to 2 weeks after the operation, but for the rest of the experiment their group mean was slightly higher than that of the control group . Table I shows that the food intake was higher for cropectomized birds than controls when given unlimited access to food, but lower when the feeding period was restricted to 2 hr or less per day . These results therefore parallel those of previous workers . The increase in ad libitum intake of the cropectomized birds and their slightly higher body weight corresponds with the increase found by Feigenbaum et al . (1962) . However, the increase in food intake is not as marked as the decrease found when intake is restricted . Experiment 2 Although cropectomy does not affect growth adversely when food is continuously available it is possible that it might produce some alteration in the pattern of feeding as an adaptation to the loss of storage capacity, The following 633
634
ANIMAL BEHAVIOUR,
18,
4
Table I . Food Intake in Grams of Sham Operated and Croptectomized Birds Under Different Feeding Schedules Sham operated N=9
Croptectomized N=8
Sham operated versus croptectomized t
96 . 4
110.8
2 .680
15
P<0.02
Restricted access to food
42 .7
27 . 3
6 . 51
15
P<0 .001
9
d
0
4
c 30
digestive tract . The average intake of the cropectomized birds in experiment 2 when allowed to feed for only 30 min was approximately 35 g . This corresponds with a volume of approximately 53 ml . It seems unlikely that this quantity of food could be passed into the proventriculusgizzard and on to the duodenum in such a period . The following experiment was carried out to determine the degree to which cropectomized animals could adapt to prolonged deprivation by increasing their intake in a test period short enough to ensure that most of the food eaten must be stored in the upper digestive tract . Methods. The cropectomized birds used in experiment 1 were tested for amount eaten in 15 min after 1 hr deprivation, and subsequently at various levels of percentage ad libitum body weight during maintained deprivation .
0
c
P
Continuous access to food
experiment was conducted to test this hypothesis . Methods. The birds used were the seventeen survivors of experiment 1 . They had continuous access to food and water . Their food intake was measured hourly from 09 .00 to 17 .00 hours. The food bins were taken out and weighed hourly for 2 days to accustom the birds to the procedure and data was collected for the subsequent 4 days . The hourly intakes for the 4 days averaged for each bird and then for each group, is shown in Fig . 1, after first being converted to percentages of the daily intake to allow for any differences in total intake . 50-
df
40 2
V 0' 2
0
17.00 09.00
09.00 10.00 10 .00 11 .00
11.00 12 .00
12 .00 13 .00
13.00 14.00
14.00 15.00 15.00 16.00
16.00 17.00
0 I c 0 100
Period (hours)
98 96 94 92 90 88 86 84 82 80
Per cent free
feeding body weight
Fig. 1 . Distribution of feeding in croptectomized and sham-operated birds . •, cropectomized (N=8) ; 0, sham-operated (N=9).
Fig. 2 . Effect of progressive deprivation on amount eaten in a 15-min test period by croptectomized birds.
Results. Cropectomy had no effect on the pattern of food intake. There were no significant differences between the groups at any of the hourly weighings during the day, nor in the amount eaten overnight. However, this experiment employed only a gross measure of food intake (weight per hour) and this may have obscured differences due to cropectomy occurring within the feeding period . Experiment 3 The above experiments indicate that under normal ad libitum conditions the crop is inessential . However it seems likely that there is some residual storage capacity in the upper
Results. Figure 2 shows that the amount eaten by the cropectomized animals increased to a maximum of over 30 g as body weight declined to 80 per cent of free-feeding weight . The birds had invariably stopped eating before the 10th min of the test period so that a large part of this quantity (45 ml) must have been still in the upper tract. Some storage capacity must remain . X-Ray Observations of the Crop Experiment 4 Von Ihnen (1928) and Fisher & Weiss (1957) both report lack of regeneration of a crop in the excised region, the latter even 18 months after the operation . It seems then that the remaining
RICHARDSON : ROLE OF CROP IN CHICKEN FEEDING BEHAVIOUR
oesophagus acts like a crop . This is possible since the oesophagus is highly distensible ; furthermore, the operation could have left untouched the sphincter mechanisms of the crop, though no effort was made to do so . To investigate this, X-ray observations were made of normal and cropectomized birds at various times after eating pellets painted with barium sulphate or being force-fed with barium sulphate paste . Previous X-ray work by Henry, Macdonald & Magee (1933) and Vonk & Postma (1949) shows that after a fast the first few boluses of food pass across the mouth of the crop and are swept directly to the gizzard and the remainder lodges in the crop . If the bird has previously been fed and the gizzard and lower tract are filled, no food passes out of the crop during eating .
63 5
oesophagus in the crop area but Fig . 3 (C) shows that pellets still clump in the region of the excised crop . Surgical excision of the crop therefore produced only a quantitative change in the function of the upper digestive tract and this is insufficient to produce obvious changes in behaviour under ad libitum feeding conditions . Artificial Distention of the Crop As an alternative to surgical removal, the function of the crop was investigated by distending it was a permanently implanted balloon cannula system, to mimic various degrees of fullness produced by normal eating . Experiment 5 Methods. Three male brown Leghorns, 10
A
B
C
CROPECTOMIZED
CROPECTOMIZED
CROPECTOMIZED
LIQUID BARIUM SULPHATE
LIQUID BARIUM SULPHATE
PELLETS
Fig. 3 . Passage of barium sulphate paste and pellets through the oesophagus of a croptectomized bird .
The barium sulphate paste showed that the amount of crop storage capacity left after the operation varied from bird to bird but was always much less than in the controls and in some birds was virtually absent : the remaining oesophagus was a straight tube with no expansion . However, even these cases showed retention of pellets in the area from which the crop had been excised . In one case the crop sphincters were seen to operate normally : a bolus was pinched off by a constriction of the oesophagus at the base of the crop and then forced onwards . Copies of three plates from one cropectomized bird are shown in Fig . 3. In Fig . 3 (A) liquid barium sulphate has been injected into the upper oesophagus and is seen passing through the crop region . In Fig . 3 (B) a large segment of the lower oesophagus, below the crop region, is contracting . Neither plate shows any expansion of the
weeks old, were prepared with implanted balloons . These were constructed from fingerstalls 25 mm long attached to a 12 mm diameter stainless steel plate, into which was fixed a 40 mm length of 20 gauge hypodermic tubing . The cannula, with the balloon attached, was pushed down the oesophagus from the mouth and out through the crop wall where it was attached by a nut. The cannula could be maintained for at least a month, and in many birds much longer. After operation the birds were adapted to a feeding schedule of 6 hr deprivation per day. The test period was the first 15 min of the 18-hr feeding period . When the amount eaten in this period was constant, the intake was measured at various levels of crop inflation in the following order : 0, 5, 25, 10 and 50 ml . The birds were then all adapted to a feeding schedule of 2 hr access each day with the first
636
ANIMAL BEHAVIOUR, 18, 4
The pattern of intake was normal as far as could be seen . The animals began eating immediately the bins were put in the cages after distention of the balloons ; there was never any suggestion that feeding was only initially suppressed and then started later in the test period as the bird adapted to the balloon, which might be expected if the inflation produced discomfort . In rats, Miller & Kessen (1954) have shown that whereas 14 ml of milk injected directly into the stomach acts as a positive reinforcer, inflation of an implanted balloon to the same extent is apparently aversive . However the balloon in the stomach is an immovable solid mass which means that when the stomach contracts it must do so virtually isometrically. The situation is quite abnormal, since normally chewed and moistened food is a semi-liquid mass which will move as one segment of the stomach contracts . By contrast, an immoveable solid mass is a normal condition in the crop immediately after eating, especially if the feeding schedule determines a large intake in a very short period. There is therefore little reason to expect a balloon in the crop to be a source of aversive stimulation, at normal inflation levels, whereas this seems quite probable for a large rigidly attached constant volume balloon in the rat stomach.
15 min of the 2-hr feeding period being the test period . Once intake in this period was stable again the birds were tested at different degrees of crop inflation as before . Results. Distention of the crop (even at 5 ml) produced a drop in food intake (Fig . 4) . At the higher level of motivation, which approximately doubled the amount eaten with zero inflation, intake was higher at all levels of distention but the general relationship remained the same. Apparently some allowance is made centrally for high levels of distention if the motivational level is high . 60
Bird I
50 403 20-
o' --: ' 60-
Bird 2
5040 -'` 30 -
1
2 10
Experiment 6 A similar procedure was carried out with three other birds tested at each inflation level after 18 hr water deprivation . The results are shown in Fig. 5 . As with food intake, increasing inflation progressively reduced the amount drunk in the 15-min test period .
0 60-0
Bird 3
50-
~'--• • 30- \ 20- -. 0 40-
Experiment 7 The work with artificial distention raised the possibility that after effects of the kind found in other sensory systems, might be produced by prolonged inflation of the crop followed by very rapid relaxation . Two birds with implanted balloons were used . They were inflated either
1o-
ao
10
20
30
40
50
Inflation (ml)
Fig. 4. Effect of crop distention by an implanted balloon upon food intake in a 15-min test period at two levels of motivation . Solid lines, low motivation ; broken lines, high motivation.
Table II. Effect of Crop Inflation on Post-inflation Eating in a 5-min Test Period Mean amount eaten after 0 nil inflation (g)
Bird
Mean amount eaten after 25 ml inflation (g)
0 ml versus 25 ml t
df
P
1
3 . 10
3-13
0-021
8
NS
2
1 .60
1 . 30
0 . 526
8
NS
RICHARDSON : ROLE OF CROP IN CHICKEN FEEDING BEHAVIOUR 100
Bird I
80 60 40 \_ 20 o'
I
I
I
I
I
I
I
100Bird 2
rn
so Y C
so
\
40 0 a
20
o I I
I
I
I I
I
Bird 3
6040200' 0
10`
15l
'
20 25
36
A
4
40 45 50
Inflation (ml)
Fig . 5 . Effect of crop distention by an implanted balloon upon water intake in a 15-min test period after 18 hr water deprivation. to 25 ml or to 0 ml and left for 30 min without food. The balloon was then deflated, the food reintroduced, and intake measured over the next 5 min . Inflations of 0 and 25 ml were alternated for a joint total of 10 days of testing and the means for each compared by t-test as shown in Table II . There was no evidence of any aftereffect of the inflation . Discussion Fisher & Weiss (1956) concluded that `the crop does not play a major role in controlling food consumption, at least on all mash diets' . The form of argument they employed, no effect of removal therefore no function, is invalid . Demonstration that an organ is completely inessential does not simultaneously demonstrate that it is completely ineffective . The usual finding in mammals is that a number of mechanisms acting `in parallel' control intake and that none taken alone is absolutely necessary ; even where there is initial impairment of control this may not be permanent ; control may come to be main-
637
tained in other ways . The same will probably be true of birds . The most obvious function of the crop is storage, though Bolton (1965) has shown that it also has some digestive and absorptive capability. The surgical removal experiments show that the storage capability is inessential so the remaining digestive tract must be able to pass sufficient food to promote normal growth . The crop may have evolved solely in response to variations in availability and nutritive density of the food supply, which modern agricultural environments explicitly prevent. In the environment of the ancestral chicken it may have acted as a buffer against short-term changes in food availability . Work by Shannon & McNab (personal communication) has shown that in animals on a 2 hr per day feeding schedule the amount of food remaining in the crop after feeding declines while the amounts in other portions of the digestive tract stay fairly constant. This raises the interesting possibility that the chicken is never metabolically hungry and may regulate its daily intake in non-metabolically related ways . The balloon experiments demonstrate that feedback of some kind is produced by distention, and this is capable of stopping feeding . Timofeev (1957) has also used crop distention as the conditioned stimulus for defensive leg lifting responses in chickens, and found that such conditioned responses are easily formed and are very much better retained than similar responses made to a light as the conditioned stimulus . Sterrit & Kienholz (1967) have mentioned briefly, without giving details of any kind, that they have prepared chicks with crop fistulas connected to a pump which delivered a purified liquid diet when the bird pecked at a key . Such chicks maintained growth within normal body weight limits, and could vary adaptively their rate of pecking when the reinforcement-to-response ratio was altered. Crop effects probably play a part in this performance but there are clearly also other sources of reinforcement . In contrast to this report, McFarland (1969) found no evidence that direct injection of water into the crop of the barbary dove can act as a reinforcer of operant behaviour. The differing results of these two studies could be due to differences in the species used, the reinforcermotivation system, or other aspects of the testing situations. In addition, until the physiological nature of the reinforcing effect is known it is not possible to know what kinds of experimental
63 8
ANIMAL BEHAVIOUR, 18, 4
manipulation are necessary to demonstrate presence or absence of reinforcement from a particular part of the digestive tract . For example, in the case of the crop, if the reinforcing effect of injected substances is due to their stimulating mucosal receptors then volume of the injection should be a trivial factor so long as there is sufficient to adequately excite such receptors. If, on the other hand the reinforcing effect is due to the injections producing a critical volume change, then the early injections, before this level is reached, are not themselves reinforcing-they will of course, become conditional reinforcers if the sequence of events is repeated often enough . In the case of the crop a reinforcing effect of the latter kind would be more likely to occur either with a very small crop as in the chick, where positive results were obtained, or with very large injections, since both these factors would mean that the critical volume was achieved quickly and there would be little delay of reinforcement . McFarland's (1969) experiment used a small injection (0 . 1 ml) which produced satiation relatively slowly. This effectively shows that crop reinforcement does not occur solely as a result of stimulation of the mucosa, and that the reinforcing effect of the same volumes by mouth does not come from the crop . It does not mean though, that part of the reinforcing effect of more rapid mouth intake does not come from the crop, or that direct injection of larger volumes into the crop would not be reinforcing, due to a mechanism based on crop volume. Paintal (1954) and Iggo (1955, 1957) have demonstrated that in cats and goats there are receptors sensitive to distention in the stomach and lower digestive tract . Fibres from these receptors run in the vagi . The response to distention may be maintained for at least a minute (Paintal 1954) and it is possible that receptors such as these in the crop play a part in the production of satiety. The motor activity of the crop is controlled by fibres running in the vagus and reaching the crop by way of the recurrent branch . Various authors have claimed that the crop shows irregularly occurring spontaneous contractions (Rogers 1916 ; Ashcroft 1930 ; Henry et al. 1933) . However, Vonk & Postma (1949) found no definite crop movements when observing its function by X-rays and suggest that the movements found by others were due to the balloon technique used . Movements of the crop under the skin can be
observed in unoperated animals but whether these actually produce major changes in crop volume such as occur with the balloon technique, is not known . Certainly, until the large `spontaneous' movements observed with implanted balloons are shown to be independent of the balloon, any attempt to treat them as a component of hunger motivation, in a manner analogous to the role postulated for the `gastric hunger pang' by Richter (1927), is pointless . Summary Surgical removal of the crop does not prevent the maintenance of normal body weight nor reduce food intake in the chicken when food is continuously available . However, when feeding time is restricted cropectomized birds eat less than normal. Cropectomy does not alter the pattern of food intake over 1-hr periods . The remaining oesophagus of cropectomized birds appears to function in some ways as a vestigial crop. Artificial inflation of the crop by a permanent balloon-cannula system decreases the amount eaten in a 15-min test period ; increased motivation leads to increased tolerance of crop inflation. No negative after-effect is apparent after prolonged inflation of the crop . Acknowledgments I wish to thank all those with whom I have discussed this work for their comments, Mrs M . Robbie of the Royal (Dick) Veterinary College, Edinburgh for taking the X-rays on which Fig. 3 is based, and Mr T . Mathieson for carrying out most of the experimental work. REFERENCES Ashcroft, D. W . (1930). The correlative activities of the alimentary canal of the fowl. Am . J. Physiol., 93, 105-110. Bolton, W. (1965) . Digestion in the crop of the fowl . Br. Poult. Sci., 6, 97-102 . Evans, A. J. (1969). Some effects of protamine zinc insulin on juvenile ducks. J. Physiol., Lond., 203, 84-86P . Farner, D . S . (1960) . Digestion and the digestive system . In : Biology and Comparative Physiology of Birds (Ed. by A . J. Marshall) . London : Academic Press . Feigenbaum, A . S ., Fisher, H. & Weiss, H. S . (1962) . Effect of `meal eating' versus `nibbling' on body composition and digestive organ weight of normal and cropectomized chickens . Am. J. clin . Nutr., 11, 312-316 . Fisher, H. & Weiss, H. S. (1956) . Food consumption in relation to dietary bulk and energy level : the effect of surgical removal of the crop . Poult. Sci., 35, 418-432. Fisher, H. & Weiss, H. S . (1957) . A further note on crop removal in the chicken . Poult. Sci., 36, 345-346.
RICHARDSON : ROLE OF CROP IN CHICKEN FEEDING BEHAVIOUR Henry, K . M ., Macdonald, A . J . & Magee, H . E. (1933) . Observations on the functions of the alimentary canal in fowls. J. exp. Biol., 10, 153-171 . Iggo, A. (1955) . Tension receptors in the stomach and the urinary bladder . J. Physiol ., Lond., 128, 593-607 . Iggo, A. (1957) . Gastro-intestinal tension receptors with afferent fibres in the vagus of the cat . Q. JI exp . Physiol., 42, 130-143 . von Ihnen, K. (1928) . Beitrage zur Physiologic des Kropfes bei Huhn and Taube. Arch . Physiol., 218, 767-796 . MacFarland, D. (1969) . Separation of satiating and rewarding consequences of drinking . Physiol. & Behav ., 4, 987-989 . Miller, N . E . & Kessen, M . L . (1954) . Is distension of the stomach by a balloon rewarding or punishing? Am . Psychol., 9, 430-431 . Paintal, A . S . (1954). A study of gastric stretch receptors . Their role in the peripheral mechanism of the
63 9
satiation of hunger and thirst . J. Physiol., Lond., 126, 255-270 . Richter, C. P. (1927) . Animal behaviour and internal drives . Q . Rev . Biol., 2, 307-343 . Rogers, F. T. (1916). Contribution to the physiology of the stomach. XXXIX . The hunger mechanism of the pigeon and its relation to the central nervous system. Am . J. Physiol., 41, 555-569. Sterrit, G . M . & Kienholz, E . (1967). Chronic pump feeding of Leghorn chicks via implanted oesophageal tubes . J. appl. Physiol., 23, 71-74. Timofeev, N. N. (1957). On the comparative physiology of exteroceptive and interoceptive conditioned reflexes . Sechenov . Physiol. J., U.S.S.R., 43, 236-242. Vonk, H . J . & Postma, N . (1949) . X-ray studies on the movements of the hen's intestine . Physiologia Comp . Oecol., 1, 15-23 . (Received 23 January 1970 ; revised 1 April 1970 ; MS. number : 943)
THE ROLE OF THE CROP IN THE FEEDING BEHAVIOUR OF THE DOMESTIC CHICKEN BY A. J . RICHARDSON A.R .C., Poultry Research Centre, King's Buildings, West Mains Road, Edinburgh 9
Although the mechanisms controlling the food intake of mammals have been extensively investigated, there has been very little comparable work on avian species . There are gross anatomical differences between the digestive tracts of mammals and birds, and also differences in metabolism, for example the reaction to insulin (Evans 1969), which suggest that there may be differences in the regulation of feeding behaviour . The experiments reported here are part of a series on various aspects of the system that controls feeding in the chicken . It is planned to include oral factors, distention mechanisms in the gut, biochemical and nutritional factors and the integration of all these in the central nervous system . The present paper is concerned solely with the part played by the crop . The size and shape of the crop varies widely between species . Farner (1960) states that it is unlikely that all the structures designated as crops are homologous . If this is so, then it is also unlikely that the part played by the crop in the control of food intake will be the same in all species. However, since it is derived in all species from the same general part of the oesophagus, which is homologous, then the basic physiology and pharmacology will probably be similar . Surgical Removal of the Crop Experiments by von Ihnen (1928) showed that presence of the crop is not necessary for the domestic chicken's survival . Later, Fisher & Weiss (1956) found that removal of the crop from 1-week-old chicks had no effect upon their subsequent weight-gain or food intake when food was continuously available . However, if feeding was restricted to two 1-hr periods per day, cropectomized birds made lower weight gains than normal controls (Feigenbaum, Fisher & Weiss 1962) . Experiment 1 Methods . This experiment was undertaken to check the findings on the effect of crop removal mentioned above . The crop was removed from ten male leghorn chicks at 1 to 2 weeks of age, by the procedure described in Fisher & Weiss
(1956) . In another ten chicks the crop was made ready for excision in the same way and the skin wound closed, leaving the crop intact . At 10 weeks the food intake of the two groups was measured under conditions of 24, 2, 11, 1 and f hr access to food per day . Data were collected over 4 days for continuous access to food and 2 days for each of the restricted-feeding periods . The data for all unrestricted and all restricted periods were averaged for each bird and the two groups compared by t-test . The rearing and housing of the birds was the same in this and subsequent experiments . They were kept in groups from hatching till 12 weeks of age and were then rehoused into single standard battery cages 28 x 40 x 45 cm. The food containers were 12 . 5 x 15 x 10 cm and spillage was very slight. All birds could see and hear other birds in the battery, which was lighted from 07 .00 to 21 .00 hours. Water was available at all times . The diet used was pelleted and had a metabolizable energy value of 2800 kcal per kg . Results. The cropectomized birds had a lower average body weight than the controls for 1 to 2 weeks after the operation, but for the rest of the experiment their group mean was slightly higher than that of the control group . Table I shows that the food intake was higher for cropectomized birds than controls when given unlimited access to food, but lower when the feeding period was restricted to 2 hr or less per day . These results therefore parallel those of previous workers . The increase in ad libitum intake of the cropectomized birds and their slightly higher body weight corresponds with the increase found by Feigenbaum et al . (1962) . However, the increase in food intake is not as marked as the decrease found when intake is restricted . Experiment 2 Although cropectomy does not affect growth adversely when food is continuously available it is possible that it might produce some alteration in the pattern of feeding as an adaptation to the loss of storage capacity, The following 633
634
ANIMAL BEHAVIOUR,
18,
4
Table I . Food Intake in Grams of Sham Operated and Croptectomized Birds Under Different Feeding Schedules Sham operated N=9
Croptectomized N=8
Sham operated versus croptectomized t
96 . 4
110.8
2 .680
15
P<0.02
Restricted access to food
42 .7
27 . 3
6 . 51
15
P<0 .001
9
d
0
4
c 30
digestive tract . The average intake of the cropectomized birds in experiment 2 when allowed to feed for only 30 min was approximately 35 g . This corresponds with a volume of approximately 53 ml . It seems unlikely that this quantity of food could be passed into the proventriculusgizzard and on to the duodenum in such a period . The following experiment was carried out to determine the degree to which cropectomized animals could adapt to prolonged deprivation by increasing their intake in a test period short enough to ensure that most of the food eaten must be stored in the upper digestive tract . Methods. The cropectomized birds used in experiment 1 were tested for amount eaten in 15 min after 1 hr deprivation, and subsequently at various levels of percentage ad libitum body weight during maintained deprivation .
0
c
P
Continuous access to food
experiment was conducted to test this hypothesis . Methods. The birds used were the seventeen survivors of experiment 1 . They had continuous access to food and water . Their food intake was measured hourly from 09 .00 to 17 .00 hours. The food bins were taken out and weighed hourly for 2 days to accustom the birds to the procedure and data was collected for the subsequent 4 days . The hourly intakes for the 4 days averaged for each bird and then for each group, is shown in Fig . 1, after first being converted to percentages of the daily intake to allow for any differences in total intake . 50-
df
40 2
V 0' 2
0
17.00 09.00
09.00 10.00 10 .00 11 .00
11.00 12 .00
12 .00 13 .00
13.00 14.00
14.00 15.00 15.00 16.00
16.00 17.00
0 I c 0 100
Period (hours)
98 96 94 92 90 88 86 84 82 80
Per cent free
feeding body weight
Fig. 1 . Distribution of feeding in croptectomized and sham-operated birds . •, cropectomized (N=8) ; 0, sham-operated (N=9).
Fig. 2 . Effect of progressive deprivation on amount eaten in a 15-min test period by croptectomized birds.
Results. Cropectomy had no effect on the pattern of food intake. There were no significant differences between the groups at any of the hourly weighings during the day, nor in the amount eaten overnight. However, this experiment employed only a gross measure of food intake (weight per hour) and this may have obscured differences due to cropectomy occurring within the feeding period . Experiment 3 The above experiments indicate that under normal ad libitum conditions the crop is inessential . However it seems likely that there is some residual storage capacity in the upper
Results. Figure 2 shows that the amount eaten by the cropectomized animals increased to a maximum of over 30 g as body weight declined to 80 per cent of free-feeding weight . The birds had invariably stopped eating before the 10th min of the test period so that a large part of this quantity (45 ml) must have been still in the upper tract. Some storage capacity must remain . X-Ray Observations of the Crop Experiment 4 Von Ihnen (1928) and Fisher & Weiss (1957) both report lack of regeneration of a crop in the excised region, the latter even 18 months after the operation . It seems then that the remaining
RICHARDSON : ROLE OF CROP IN CHICKEN FEEDING BEHAVIOUR
oesophagus acts like a crop . This is possible since the oesophagus is highly distensible ; furthermore, the operation could have left untouched the sphincter mechanisms of the crop, though no effort was made to do so . To investigate this, X-ray observations were made of normal and cropectomized birds at various times after eating pellets painted with barium sulphate or being force-fed with barium sulphate paste . Previous X-ray work by Henry, Macdonald & Magee (1933) and Vonk & Postma (1949) shows that after a fast the first few boluses of food pass across the mouth of the crop and are swept directly to the gizzard and the remainder lodges in the crop . If the bird has previously been fed and the gizzard and lower tract are filled, no food passes out of the crop during eating .
63 5
oesophagus in the crop area but Fig . 3 (C) shows that pellets still clump in the region of the excised crop . Surgical excision of the crop therefore produced only a quantitative change in the function of the upper digestive tract and this is insufficient to produce obvious changes in behaviour under ad libitum feeding conditions . Artificial Distention of the Crop As an alternative to surgical removal, the function of the crop was investigated by distending it was a permanently implanted balloon cannula system, to mimic various degrees of fullness produced by normal eating . Experiment 5 Methods. Three male brown Leghorns, 10
A
B
C
CROPECTOMIZED
CROPECTOMIZED
CROPECTOMIZED
LIQUID BARIUM SULPHATE
LIQUID BARIUM SULPHATE
PELLETS
Fig. 3 . Passage of barium sulphate paste and pellets through the oesophagus of a croptectomized bird .
The barium sulphate paste showed that the amount of crop storage capacity left after the operation varied from bird to bird but was always much less than in the controls and in some birds was virtually absent : the remaining oesophagus was a straight tube with no expansion . However, even these cases showed retention of pellets in the area from which the crop had been excised . In one case the crop sphincters were seen to operate normally : a bolus was pinched off by a constriction of the oesophagus at the base of the crop and then forced onwards . Copies of three plates from one cropectomized bird are shown in Fig . 3. In Fig . 3 (A) liquid barium sulphate has been injected into the upper oesophagus and is seen passing through the crop region . In Fig . 3 (B) a large segment of the lower oesophagus, below the crop region, is contracting . Neither plate shows any expansion of the
weeks old, were prepared with implanted balloons . These were constructed from fingerstalls 25 mm long attached to a 12 mm diameter stainless steel plate, into which was fixed a 40 mm length of 20 gauge hypodermic tubing . The cannula, with the balloon attached, was pushed down the oesophagus from the mouth and out through the crop wall where it was attached by a nut. The cannula could be maintained for at least a month, and in many birds much longer. After operation the birds were adapted to a feeding schedule of 6 hr deprivation per day. The test period was the first 15 min of the 18-hr feeding period . When the amount eaten in this period was constant, the intake was measured at various levels of crop inflation in the following order : 0, 5, 25, 10 and 50 ml . The birds were then all adapted to a feeding schedule of 2 hr access each day with the first
636
ANIMAL BEHAVIOUR, 18, 4
The pattern of intake was normal as far as could be seen . The animals began eating immediately the bins were put in the cages after distention of the balloons ; there was never any suggestion that feeding was only initially suppressed and then started later in the test period as the bird adapted to the balloon, which might be expected if the inflation produced discomfort . In rats, Miller & Kessen (1954) have shown that whereas 14 ml of milk injected directly into the stomach acts as a positive reinforcer, inflation of an implanted balloon to the same extent is apparently aversive . However the balloon in the stomach is an immovable solid mass which means that when the stomach contracts it must do so virtually isometrically. The situation is quite abnormal, since normally chewed and moistened food is a semi-liquid mass which will move as one segment of the stomach contracts . By contrast, an immoveable solid mass is a normal condition in the crop immediately after eating, especially if the feeding schedule determines a large intake in a very short period. There is therefore little reason to expect a balloon in the crop to be a source of aversive stimulation, at normal inflation levels, whereas this seems quite probable for a large rigidly attached constant volume balloon in the rat stomach.
15 min of the 2-hr feeding period being the test period . Once intake in this period was stable again the birds were tested at different degrees of crop inflation as before . Results. Distention of the crop (even at 5 ml) produced a drop in food intake (Fig . 4) . At the higher level of motivation, which approximately doubled the amount eaten with zero inflation, intake was higher at all levels of distention but the general relationship remained the same. Apparently some allowance is made centrally for high levels of distention if the motivational level is high . 60
Bird I
50 403 20-
o' --: ' 60-
Bird 2
5040 -'` 30 -
1
2 10
Experiment 6 A similar procedure was carried out with three other birds tested at each inflation level after 18 hr water deprivation . The results are shown in Fig. 5 . As with food intake, increasing inflation progressively reduced the amount drunk in the 15-min test period .
0 60-0
Bird 3
50-
~'--• • 30- \ 20- -. 0 40-
Experiment 7 The work with artificial distention raised the possibility that after effects of the kind found in other sensory systems, might be produced by prolonged inflation of the crop followed by very rapid relaxation . Two birds with implanted balloons were used . They were inflated either
1o-
ao
10
20
30
40
50
Inflation (ml)
Fig. 4. Effect of crop distention by an implanted balloon upon food intake in a 15-min test period at two levels of motivation . Solid lines, low motivation ; broken lines, high motivation.
Table II. Effect of Crop Inflation on Post-inflation Eating in a 5-min Test Period Mean amount eaten after 0 nil inflation (g)
Bird
Mean amount eaten after 25 ml inflation (g)
0 ml versus 25 ml t
df
P
1
3 . 10
3-13
0-021
8
NS
2
1 .60
1 . 30
0 . 526
8
NS
RICHARDSON : ROLE OF CROP IN CHICKEN FEEDING BEHAVIOUR 100
Bird I
80 60 40 \_ 20 o'
I
I
I
I
I
I
I
100Bird 2
rn
so Y C
so
\
40 0 a
20
o I I
I
I
I I
I
Bird 3
6040200' 0
10`
15l
'
20 25
36
A
4
40 45 50
Inflation (ml)
Fig . 5 . Effect of crop distention by an implanted balloon upon water intake in a 15-min test period after 18 hr water deprivation. to 25 ml or to 0 ml and left for 30 min without food. The balloon was then deflated, the food reintroduced, and intake measured over the next 5 min . Inflations of 0 and 25 ml were alternated for a joint total of 10 days of testing and the means for each compared by t-test as shown in Table II . There was no evidence of any aftereffect of the inflation . Discussion Fisher & Weiss (1956) concluded that `the crop does not play a major role in controlling food consumption, at least on all mash diets' . The form of argument they employed, no effect of removal therefore no function, is invalid . Demonstration that an organ is completely inessential does not simultaneously demonstrate that it is completely ineffective . The usual finding in mammals is that a number of mechanisms acting `in parallel' control intake and that none taken alone is absolutely necessary ; even where there is initial impairment of control this may not be permanent ; control may come to be main-
637
tained in other ways . The same will probably be true of birds . The most obvious function of the crop is storage, though Bolton (1965) has shown that it also has some digestive and absorptive capability. The surgical removal experiments show that the storage capability is inessential so the remaining digestive tract must be able to pass sufficient food to promote normal growth . The crop may have evolved solely in response to variations in availability and nutritive density of the food supply, which modern agricultural environments explicitly prevent. In the environment of the ancestral chicken it may have acted as a buffer against short-term changes in food availability . Work by Shannon & McNab (personal communication) has shown that in animals on a 2 hr per day feeding schedule the amount of food remaining in the crop after feeding declines while the amounts in other portions of the digestive tract stay fairly constant. This raises the interesting possibility that the chicken is never metabolically hungry and may regulate its daily intake in non-metabolically related ways . The balloon experiments demonstrate that feedback of some kind is produced by distention, and this is capable of stopping feeding . Timofeev (1957) has also used crop distention as the conditioned stimulus for defensive leg lifting responses in chickens, and found that such conditioned responses are easily formed and are very much better retained than similar responses made to a light as the conditioned stimulus . Sterrit & Kienholz (1967) have mentioned briefly, without giving details of any kind, that they have prepared chicks with crop fistulas connected to a pump which delivered a purified liquid diet when the bird pecked at a key . Such chicks maintained growth within normal body weight limits, and could vary adaptively their rate of pecking when the reinforcement-to-response ratio was altered. Crop effects probably play a part in this performance but there are clearly also other sources of reinforcement . In contrast to this report, McFarland (1969) found no evidence that direct injection of water into the crop of the barbary dove can act as a reinforcer of operant behaviour. The differing results of these two studies could be due to differences in the species used, the reinforcermotivation system, or other aspects of the testing situations. In addition, until the physiological nature of the reinforcing effect is known it is not possible to know what kinds of experimental
63 8
ANIMAL BEHAVIOUR, 18, 4
manipulation are necessary to demonstrate presence or absence of reinforcement from a particular part of the digestive tract . For example, in the case of the crop, if the reinforcing effect of injected substances is due to their stimulating mucosal receptors then volume of the injection should be a trivial factor so long as there is sufficient to adequately excite such receptors. If, on the other hand the reinforcing effect is due to the injections producing a critical volume change, then the early injections, before this level is reached, are not themselves reinforcing-they will of course, become conditional reinforcers if the sequence of events is repeated often enough . In the case of the crop a reinforcing effect of the latter kind would be more likely to occur either with a very small crop as in the chick, where positive results were obtained, or with very large injections, since both these factors would mean that the critical volume was achieved quickly and there would be little delay of reinforcement . McFarland's (1969) experiment used a small injection (0 . 1 ml) which produced satiation relatively slowly. This effectively shows that crop reinforcement does not occur solely as a result of stimulation of the mucosa, and that the reinforcing effect of the same volumes by mouth does not come from the crop . It does not mean though, that part of the reinforcing effect of more rapid mouth intake does not come from the crop, or that direct injection of larger volumes into the crop would not be reinforcing, due to a mechanism based on crop volume. Paintal (1954) and Iggo (1955, 1957) have demonstrated that in cats and goats there are receptors sensitive to distention in the stomach and lower digestive tract . Fibres from these receptors run in the vagi . The response to distention may be maintained for at least a minute (Paintal 1954) and it is possible that receptors such as these in the crop play a part in the production of satiety. The motor activity of the crop is controlled by fibres running in the vagus and reaching the crop by way of the recurrent branch . Various authors have claimed that the crop shows irregularly occurring spontaneous contractions (Rogers 1916 ; Ashcroft 1930 ; Henry et al. 1933) . However, Vonk & Postma (1949) found no definite crop movements when observing its function by X-rays and suggest that the movements found by others were due to the balloon technique used . Movements of the crop under the skin can be
observed in unoperated animals but whether these actually produce major changes in crop volume such as occur with the balloon technique, is not known . Certainly, until the large `spontaneous' movements observed with implanted balloons are shown to be independent of the balloon, any attempt to treat them as a component of hunger motivation, in a manner analogous to the role postulated for the `gastric hunger pang' by Richter (1927), is pointless . Summary Surgical removal of the crop does not prevent the maintenance of normal body weight nor reduce food intake in the chicken when food is continuously available . However, when feeding time is restricted cropectomized birds eat less than normal. Cropectomy does not alter the pattern of food intake over 1-hr periods . The remaining oesophagus of cropectomized birds appears to function in some ways as a vestigial crop. Artificial inflation of the crop by a permanent balloon-cannula system decreases the amount eaten in a 15-min test period ; increased motivation leads to increased tolerance of crop inflation. No negative after-effect is apparent after prolonged inflation of the crop . Acknowledgments I wish to thank all those with whom I have discussed this work for their comments, Mrs M . Robbie of the Royal (Dick) Veterinary College, Edinburgh for taking the X-rays on which Fig. 3 is based, and Mr T . Mathieson for carrying out most of the experimental work. REFERENCES Ashcroft, D. W . (1930). The correlative activities of the alimentary canal of the fowl. Am . J. Physiol., 93, 105-110. Bolton, W. (1965) . Digestion in the crop of the fowl . Br. Poult. Sci., 6, 97-102 . Evans, A. J. (1969). Some effects of protamine zinc insulin on juvenile ducks. J. Physiol., Lond., 203, 84-86P . Farner, D . S . (1960) . Digestion and the digestive system . In : Biology and Comparative Physiology of Birds (Ed. by A . J. Marshall) . London : Academic Press . Feigenbaum, A . S ., Fisher, H. & Weiss, H. S . (1962) . Effect of `meal eating' versus `nibbling' on body composition and digestive organ weight of normal and cropectomized chickens . Am. J. clin . Nutr., 11, 312-316 . Fisher, H. & Weiss, H. S. (1956) . Food consumption in relation to dietary bulk and energy level : the effect of surgical removal of the crop . Poult. Sci., 35, 418-432. Fisher, H. & Weiss, H. S . (1957) . A further note on crop removal in the chicken . Poult. Sci., 36, 345-346.
RICHARDSON : ROLE OF CROP IN CHICKEN FEEDING BEHAVIOUR Henry, K . M ., Macdonald, A . J . & Magee, H . E. (1933) . Observations on the functions of the alimentary canal in fowls. J. exp. Biol., 10, 153-171 . Iggo, A. (1955) . Tension receptors in the stomach and the urinary bladder . J. Physiol ., Lond., 128, 593-607 . Iggo, A. (1957) . Gastro-intestinal tension receptors with afferent fibres in the vagus of the cat . Q. JI exp . Physiol., 42, 130-143 . von Ihnen, K. (1928) . Beitrage zur Physiologic des Kropfes bei Huhn and Taube. Arch . Physiol., 218, 767-796 . MacFarland, D. (1969) . Separation of satiating and rewarding consequences of drinking . Physiol. & Behav ., 4, 987-989 . Miller, N . E . & Kessen, M . L . (1954) . Is distension of the stomach by a balloon rewarding or punishing? Am . Psychol., 9, 430-431 . Paintal, A . S . (1954). A study of gastric stretch receptors . Their role in the peripheral mechanism of the
63 9
satiation of hunger and thirst . J. Physiol., Lond., 126, 255-270 . Richter, C. P. (1927) . Animal behaviour and internal drives . Q . Rev . Biol., 2, 307-343 . Rogers, F. T. (1916). Contribution to the physiology of the stomach. XXXIX . The hunger mechanism of the pigeon and its relation to the central nervous system. Am . J. Physiol., 41, 555-569. Sterrit, G . M . & Kienholz, E . (1967). Chronic pump feeding of Leghorn chicks via implanted oesophageal tubes . J. appl. Physiol., 23, 71-74. Timofeev, N. N. (1957). On the comparative physiology of exteroceptive and interoceptive conditioned reflexes . Sechenov . Physiol. J., U.S.S.R., 43, 236-242. Vonk, H . J . & Postma, N . (1949) . X-ray studies on the movements of the hen's intestine . Physiologia Comp . Oecol., 1, 15-23 . (Received 23 January 1970 ; revised 1 April 1970 ; MS. number : 943)