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Gastric motility in great horned owls (Bubo virginianus)
Camp. Biochem. Physiol., 1975, Vol. 51A, pp. 201 to 205. Pergamon Press. Printed in Great Britain
GASTRIC
MOTILITY
IN GREAT HORNED VIRGINIANUS)”
OWLS (BUBO
T. E. KOSTUCH AND G. E. DUKE Department
of Veterinary Biology, College of Veterinary Medicine, University of Minnesota, St. Paul, Minnesota 55101, U.S.A. (Received
21 January
1974)
Abstract-l. The mean amplitude of gastric pressure changes (94.3 mm Hg) was considerably greater than anticipated from previous reports. 2. Three phases in the digestion of a meal were apparent from records of gastric pressure changes. The phases were termed the mechanical digestion phase, chemical digestion phase and pellet formation and egestion phase. Contraction frequency was greatest during the first phase while contraction amplitude was greatest during the third phase. The lengths of the phases varied with the quantity eaten by an owl. 3. The gastroduodenal contraction sequence began in the glandular stomach, then the muscular stomach and lastly the duodenum. In the muscular stomach, contractions began adjacent to the gastric isthmus and proceeded around the circumference of the muscular stomach to the pylorus.
INTRODUCTION THERE is little information available describing gastric motility of raptors. Mangold (1971) measured the pressure changes in the muscular stomach of the mouse buzzard (Bureo buteo) using a balloon/manometer technique. Reed & Reed (1928), using fluoroscopy, described the contraction sequence of the smooth muscles of the muscular stomach of the great homed owl. The purposes of this investigation were to study gastric pressure changes via pressure telemetry for the period from eating until pellet egestion, and to describe the gastroduodenal contraction cycle of the great
horned owl. MATERIALS AND METHODS Four adult great homed owls were used. They were kept in a room in which the temperature, relative humidity and photoperiod were controlled and were fed a diet of mice. Gastric pressures were detected by a radio telemetry transmitter (Airborne Model 430 pressure transender, Airborne Instrument Laboratories, Deer Park, NY) which was inserted into a mouse, fed to an owl therein and subsequently retrieved from the egested pellet. The transmitter was of cylindrical shape 0.8 cm in dia. and 2.5 cm in length. Prior to the initiation of experiments involving feeding of the transmitter to owls, a piece of plastic tubing with the same dimensions as the transmitter was fed to determine whether an object of this size would be harmed by, or, have any harmful affects on, the owls. The feeding of this tubing apparently did not affect the owls. Their behaviour, food intake and the nature of their excreta and pellets all appeared to be normal. * This study was partially supported by National Science Foundation Grant No. NSF-GB37254.
The transmitter transmitted at a center frequency of 2 MHz. The frequency of the transmitted signal varied in response to pressure changes exerted on the transmitter. The maximum variation of the signal was 50 kHz. The signal was received (Airborne Model 435 Receiver) and then transferred to a two-channel recorder (Hewlett-Packard Model 7402A, Hewlett-Packard, San Diego, CA) with high gain d.c. preamplifiers (HewlettPackard Model 17400A). Calibration of the transmitter, receiver and recorder was accomplished just prior to feeding the transmitter to an owl. For calibration, the transmitter was placed into a tlask in a water-bath and heated to normal body temperature of the great homed owl (39°C). Known pressures were applied to the flask causing a change in the frequency of the transmitted signal. The receiver gain was adjusted so that a given applied pressure change resulted in a predictable deflcction of the writing arm of the recorder. The owls were fed their normal diet plus the transmitter between 1500 and 1600 hours each day. The transmitted signal was recorded until a pellet containing the transmitter was egested g-20.5 hr later. Amplitudes anddurationsof contractionswereanalyzed for 1 min of every 5 min of the pressure records. The number of contractions per min (frequency) was determined from the entire 5-min period. Mean values for frequency, duration and amplitude of pressure changes were calculated for one-half hour periods and plotted on graphs for each experiment (e.g. Fig. 2). By visual inspection of each graph the data were divided into three parts representing what we theorized to be three phases of digestion. All of the data from each experiment were further assigned to one of three groups based on the quantity eaten by the owl during that experiment. Then, means for frequency duration and amplitude of pressure changes were determined for each phase of digestion for each group of experiments in which similar quantities were eaten (Table 1). 201
T. E. KOSTUCHAND G. E. DUKE
202
Table 1. Mean amplitude, frequency and duration of gastric intraluminal pressure changes during gastric digestion of three weight classes of mouse meals in great horned owls Weight class of meal (g)
No. of trials
20-40
4
90.3 (52.2)t
58.2 (38.1)
174.1 (841)
(;.:).
60-85
8
71.2 (40.9)
53.6 (78.0)
157.4 (272.1)
(G)
100+
4
Amplitude (mm Hg) I* 11* 111*
Frequency (No./min) I II III
(A::,
I
Duration (XC) II III
(Z)
23.1 (9.0)
23.7 (11.4)
19.3 (8.6)
(&
23.9 (58)
34.9 (32.5)
18.0 (9.3)
1.7 (0.4)
* The numbers I, II, III refer to three phases of gastric digestion, mechanical digestion and pellet formation and egestion. t Numbers in parentheses are standard deviations.
20-409
digestion, chemical
60-R5g I
Exp.4.0~
ICI
260 240 220 0,
200 180
E E
160 140 120 100
I
f a
,““o 40 20
.r E
‘-, 0, 3
:
t4
20 I-5 I.0 0.5 I
2 4
6
8 IO 12 I4 16 I8
2 4
6 8 IO I2 I4 16
,
,
2 4
6
I
I
I
I
I
/
L
8 IO 12 14 16 18 20
Hours
Fig. 2. Averages of amplitudes, frequencies and durations of gastric pressure changes for one-half hour periods from food ingestion to pellet egestion for three typical experiments with great homed owls. A different quantity of mice was eaten by the test owl in each experiment. C, The start of the chemical digestion phase; P, the start of the pellet formation and egestion phase. (Phases were determined by inspection of records.)
Four criteria were used for dividing data on pressure changes into three parts to designate three phases of digestion. The first phase began when food (and the transmitter) was ingested. The point at whiih amplitudes and frequencies began a major, persistent decrease and durations began a similar but opposite increase was chosen as the end of phase one and the start of phase two. The end of phase two and the start of phase three was believed to occur when amplitude and frequency each began a major, persistent increase and duration began to decrease. Pellet egestion was considered to be the end of
phase three. These points were normally apparent on the graphs from the separate experiments (e.g. Fig. 2). To study the gastroduodenal contraction sequence of the great homed owl a radiographic unit (Emperor 90/l 5 table, 6-in. image intensifier, 825 line split TV, 35 mm tine, Jupiter 90 MA control and transformer, Profexray, Des Plaines, IL) was used which consisted of components which allowed both monitoring by closed-circuit television and recording on 35 mm film (double x negative film, Type 5222, DKN 718, Eastman Kodak Co., Oak Brook, IL). Barium sulfate (Barosperse, Mallinckrodt Chemical Works, St. Louis, MO) was used as a constrast
Fig. la (upper). A series (A-E) of cineradiographic prints of a typical gastric contraction sequence in the muscular stomach of a great horned owl. The white line and arrow indicate the area undergoing contraction in each print. I, Gastric isthmus; P, pylorus; M, muscular stomach; S, small intestine; L, large intestine. Fig. I b (lower). Examples of typical intragastric pressure tracings of dicrotic (I), tricrotic (II) and biphasic (III) pressure waves. The letters A-E indicate the nature of the intragastric pressures occurring in response to contraction of each area (a+, Fig. la) of the muscular stomach. This relationship was determined by simultaneously recording intragastric pressures and radiographically observing gastric motility.
Gastric motility in great homed owls medium. It was force-fed as an aqueous suspension or it was injected into a mouse before the mouse was fed to an
owl. The presence of the telemetry transmitter during radiographic observations also aided in analysis of the gastroduodenal sequence and allowed correlation of the recorded pressure changes with the gastric contraction sequence seen radiographically. RESULTS
The pressures recorded ranged from 10 to 350 mm Hg in amplitude and averaged 943 mm Hg. Contraction frequency, throughout the recording periods, ranged from @4 to 3.0 c/min averaging 1-3 c/min. The duration of the contractions varied inversely with the frequency of contractions ranging from 5.0 to 63.0 set and averaging 24.0 sec. The wave form on the records of pressure changes was highly variable. Biphasic and triphasic, as well as dicrotic and tricrotic waves, were observed (Fig. 1). No single wave form was characteristic of any period within the record. As indicated above, when the amplitudes, frequencies and durations of pressure changes (i.e. contractions) were plotted against time, patterns which could be divided into three phases were apparent (Fig. 2). The first phase, which we have termed the phase of mechanical digestion, started immediately after eating. During this phase contraction frequency was higher than during the other two phases and averages for durations and amplitudes of contractions were intermediate to the averages for these parameters during the other two phases (Table 1). We have called the second phase the phase of chemical digestion. During this phase the contraction frequencies and amplitudes were lower and the durations were somewhat longer than during the other two phases (Table 1; Fig. 2). The third phase was called the phase of pellet formation and egestion. During this phase, the amplitude of contractions was the highest of all three phases and durations of contractions were the shortest of the three phases (Table 1; Fig. 2). In general, the average frequency of contractions during the third phase was intermediate to this average for the other two phases. During the study it became evident that the nature of gastric pressure records varied according to the
203
quantity eaten by a test owl. Thus, records were divided into three groups on the basis of quantity eaten. In general, the lengths of the three phases increased and their post-prandial starting times became later as the quantity eaten increased. As a result, the interval of time between eating and pellet egestion was also longer when a larger quantity was eaten. The mean meal-to-pellet time interval when 20-40 g were eaten was 12.8 hr (s = + 2.9). When 60-85 g were eaten this mean was 145 hr (S = + 2.5) and when 100 g or more were consumed by an owl the average meal-to-pellet interval was 185 hr (s = k2.2). Regardless of the amount eaten, amplitudes of pressure changes normally declined just prior to pellet egestion (Fig. 2). And, during the final 6-8 min prior to egestion, the amplitudes declined to less than 10 mm Hg (Table 2). The three phases of digestion were approximately equally apparent from graphs of frequency, duration and amplitude of pressure changes regardless of the quantity eaten (Fig. 2). Amplitude of contractions varied inversely with the amount eaten; however, the frequency of contractions increased with the increased amount fed. Duration of the contractions remained relatively constant regardless of the amount eaten (Fig. 2; Table 1). The gastroduodenal contraction sequence, observed primarily during phases one and two, began with a peristaltic wave of contraction moving down the glandular stomach. This was followed by a contraction sequence in the muscular stomach in which a contraction began near the isthmus and proceeded around the greater curvature of the muscular stomach to the pylorus (Fig. 1). The contraction of the duodenum began just as the contraction wave in the muscular stomach reached the pylorus. A duodenal contraction wave, as observed radiographically, rapidly moved contents throughout the duodenum. By simultaneously recording gastric pressure changes and observing gastric contractions radiographically, it was possible to correlate the development of a pressure wave with the contraction sequence of the muscular stomach. The start of the contraction sequence near the isthmus correlated with the beginning of the pressure wave. Maximum pressure was recorded during the time at which the
Table 2. Amplitudes of pressure changes recorded from the stomach or esophagus of a great homed owl during the 8nal 8 tin prior to egestion of a pellet Time prior to egestion (min) 8-7
7-6
6-5
5-4
4-3
3-2
2-1
Mean (mm Hg)
15.0
11.3
127
S.D.* (mm Hg)
14.9
N
11
11.6 7.8 13
9.9 6.2 14
8.4 6.5 14
6.9 48 13
* SD., Standard deviation.
8.9
12
7.9
13
1-O
7.2 5.3 13
T. E. KOSTUCHAND G. E.
204
contraction wave was about halfway between the isthmus and pylorus. Pressure had returned to the baseline value when the contraction wave arrived at the pylorus (Fig. 1). DISCUSSION
Mangold (1911) recorded gastric pressure changes in a mouse buzzard at 05-l hr after eating. These pressure changes ranged from 8 to 20 mm Hg in amplitude and occurred at a rate of approximately 3 c/min. At a similar postprandial time, amplitudes of pressure changes reported herein averaged three to five times more than the maximum amplitude reported by Mangold. The average frequency of pressure changes was, however, less throughout the present study than the frequency reported by Mangold. In Mangold’s experiments intragastric pressures were studied by passing a balloon into the muscular stomach per OS. The mouse buzzard was restrained during the recording experiment. Perhaps these procedures inhibited the amplitude of gastric motility in the buzzard while the presence of the balloon in the birds’ stomach may have simultaneously stimulated gastric contraction frequency. On the other hand, amplitudes and frequencies of gastric pressure changes recorded by Mangold may have been unaffected by the procedures used and the mouse buzzard may indeed have had a lower amplitude and a higher frequency of gastric pressure changes than the great horned owl. Chemical digestion is apparently more thorough in hawks than in owls (Duke et al., 1975), so the amplitude of gastric pressures may be greater in owls to compensate for poorer chemical digestion. Mean amplitudes of pressure changes recorded in this study were comparable to those reported for poultry. Mean amplitudes of pressures resulting from contraction of the thick muscles of the muscular stomach in turkeys and chickens were 62 and 180 mm Hg, respectively (Duke et al., 1972). Muscles of the muscular stomach of poultry are two to three times thicker than those of the great horned owl and one might, therefore, expect to record pressure changes of greater amplitude from poultry. The gastric contraction sequence of great horned owls reported in this study and previously reported by Reed & Reed (1928) is very much different from that of turkeys (Dziuk & Duke, 1972); This difference is probably accounted for by the fact that the gross anatomy of the muscular stomach of raptors and galliforms is likewise very diss.imilar (Farner, 1960). Raptors lack the paired thick and thin muscles of the muscular stomach (Dziuk & Duke, 1972) of .galliform birds. Morever, the entire gastroduodenal contraction cycle is also different for these two groups of birds. In galliforms the thin muscles of the muscular stomach contract first in the gastroduodenal contraction sequence, then the
DUKE
duodenum, next the thick muscles of the muscular stomach and lastly the glandular stomach (Nolf, 1938a, b; Dziuk &Duke, 1972). The gastroduodenal contraction sequence described herein for owls has not been previously detailed for raptors. These anatomical and functional differences between raptors and galliforms are apparently related to their different food habits. Since amplitudes of pressures occurring in the muscular stomach of great horned owls and poultry are similar, the contraction pattern of the muscular stomach must be more important in mechanical digestion than the pressure generated by muscular stomach contractions. Apparently the gastric contraction sequence in fowl is more appropriate for grinding grain than the more simple sequence seen in the muscular stomach of the owl. Distinct phases in the digestion of a meal have not been previously reported for birds. In addition, reports of long-term recording of gastric motility in birds, as described herein, could not be found. The four phases in rumination (Phillipson, 1970) and the filling, mechanical digestion and emptying phenomena in the gastric digestion of a meal in mammals with simple stomachs (Hightower, 1966) are not comparable to the phases described herein. As the names selected for the three phases described herein suggest, these phases in gastric motility probably represent stages in the gastric digestion of a meal. It is hypothesized that food is primarily crushed and macerated and then mixed with gastric secretions during the first, or mechanical digestion phase. During the second, or chemical digestion phase, low-amplitude contractions probably gently mix ingesta with gastric digestive secretions. A great deal of gastric digestion probably occurs during this phase. It is likely that soft tissues are digested from bones and broken into very small particles which can be emptied from the muscular stomach during the second phase, but it is doubtful that much ingesta is emptied at that time. During the phase of pellet formation and egestion, fluid ingesta are probably emptied from the stomach by the high amplitude contractions characteristic of that phase. These contractions probably also compact the remaining hair and bones into a pellet. It is possible that the process of pellet egestion is more comparable to regurgitation than to emesis. Pressures recorded during the last few minutes prior to egestion are very low in amplitude which would indicate that the high amplitude intragastric pressures characteristic of emesis (Hightower, 1966) were not occurring. Regurgitation of ingesta as a normal regularly recurring physiological process is characteristic of ruminants (Anderson & Jones, 1967) but apparently ,does not .occur normally in other mammals. Lengths of the three phases observed in this investigation, overa& meaLto-pellet interval and post-prandial starting time of each phase varied with
Gastric motility in great homed owls the quantity eaten. This variation was apparent from graphs of either frequency, duration or amplitude of gastric pressure changes. Therefore, if one could transmit information on gastric motility in a free-living great horned owl, using long-range radiotelemetry, the amount eaten by the owl could be estimated. Pellet egestion should be detected by this system also. By pinpointing the position of the owl at the time of egestion, many pellets could be collected and the nature of the meal responsible for the pellet could be determined. This system would provide valuable information on energetics of great horned owls. SUMMABY Gastric motility was studied in four great horned owls by intragastric pressure telemetry and by radiographic observation. Amplitudes, frequencies and durations of gastric pressure changes averaged 94.3 mm Hg, 1.3 c/mm and 24.0 set, respectively. Amplitudes, frequencies and durations of gastric pressure changes varied during the gastric digestion of a meal in such a way that three successive phases of gastric digestion were apparent from pressure records. These phases were called the mechanical digestion phase, chemical digestion phase and pellet formation and egestion phase. Contraction frequency was greatest during the first phase while contraction amplitude was greatest during the third phase. Lengths of the phases and overall meal-topellet time interval increased as the quantity eaten by an owl increased. The gastroduodenal contraction sequence was observed radiographically to begin in the glandular stomach. Contractions then proceeded into and through the muscular stomach and finally on into the duodenum. In the muscular stomach the contraction cycle began adjacent to the gastric isthmus and proceeded around the circumference of the muscular stomach to the pylorus.
205
staff at the Veteran’s Administration Hospital, Mirmeapolis, Minnesota, particularly Dr. U. S. Seal, Mrs. D. Gaiser and Mr. T. Stoebe, in making cineradiographic equipment available to us was greatly appreciated. We are very grateful to Mr. Jerry Schlegel of the Mayo Clinic, Rochester, Minnesota, for the temporary loan of a telemetry transmitter which enabled us to fmish our study. REFERENCES
ANDERSON S. & JONESJ. K., JR. (1967) Recent Mammals ofthe World, p. 402. Ronald Press, New York. DUKE G. E., Dzrurc H. E. & EVANXIN0. A. (1972) Gastric pressure and smooth muscle electrical potential changes in turkeys. Am.J. Physiol. 222,167-173. DUKE G. E., JEGERSA. A., LOFFG. & EVAN.WN0. A. (1975) Gastric digestion in some raptors. Comp. Biochem. Physiol. (In preparation.) Dzru~ H. E. & DUKE G. E. (1972) Cineradiographic studies of gastric motility in turkeys. Am. J. Physiol. 222,159-166. FARNERD.
S. (1960) The digestive system and digestion. In Biology and Comparative Physiology of Birds (Edited by MARSHALLA. J.), Vol. I, pp. 411-467. Academic Press, New York. HIGHTOWERN. C. (1966) Movements of the alimentary canal. In The Physiological Basis of Medical Practice (Edited by BELTC. H. & TAYLORN. B.), 8th Edn., pp. 1196-1241. Williams &Wilkins, Baltimore. MANGOLDE. (1911) Die funktionellen Schwankungen der motor&hen Tatigkeit des Raubvogelmagens. Ppiger ‘s Arch. ges. Physiol. 139,10-32. NOLF
P. (1938a) L’appareil nerveux de l’automatisme gastrique de l’oiseau-I. Essai d’analyse par la nicotine. Archs int. Physiol. 46,1-85. NOLF P. (1938b) L’aonareil nerveux de l’automatisme gastriquk de Boise&-II. Etude des effets causes par une ou plusieurs sections de l’anneau nerveux du gesier. Archs int. Physiol. 46,441-559. PHILLIPSON A.
T. (1970) Ruminant digestion. In Dukes’ Physiology of Domestic Animals (Edited by SWENWN
M. J.), 8th Edn., pp. 424483. Cornell University Press, Ithaca. REEDC. I. & REEDB. P. (1928) The mechanism of pellet formation in the great homed owl (Babe virginianus). Science, Wash. 68,359-360.
authors are grateful for technical assistance from Miss A. A. Jegers and Mr. D. D. Rhoades throughout the study. The help of the research Acknowledgements-The
Key Word Index-Raptor; motility; gastric motility.
owl; owl digestion; GI
GASTRIC
MOTILITY
IN GREAT HORNED VIRGINIANUS)”
OWLS (BUBO
T. E. KOSTUCH AND G. E. DUKE Department
of Veterinary Biology, College of Veterinary Medicine, University of Minnesota, St. Paul, Minnesota 55101, U.S.A. (Received
21 January
1974)
Abstract-l. The mean amplitude of gastric pressure changes (94.3 mm Hg) was considerably greater than anticipated from previous reports. 2. Three phases in the digestion of a meal were apparent from records of gastric pressure changes. The phases were termed the mechanical digestion phase, chemical digestion phase and pellet formation and egestion phase. Contraction frequency was greatest during the first phase while contraction amplitude was greatest during the third phase. The lengths of the phases varied with the quantity eaten by an owl. 3. The gastroduodenal contraction sequence began in the glandular stomach, then the muscular stomach and lastly the duodenum. In the muscular stomach, contractions began adjacent to the gastric isthmus and proceeded around the circumference of the muscular stomach to the pylorus.
INTRODUCTION THERE is little information available describing gastric motility of raptors. Mangold (1971) measured the pressure changes in the muscular stomach of the mouse buzzard (Bureo buteo) using a balloon/manometer technique. Reed & Reed (1928), using fluoroscopy, described the contraction sequence of the smooth muscles of the muscular stomach of the great homed owl. The purposes of this investigation were to study gastric pressure changes via pressure telemetry for the period from eating until pellet egestion, and to describe the gastroduodenal contraction cycle of the great
horned owl. MATERIALS AND METHODS Four adult great homed owls were used. They were kept in a room in which the temperature, relative humidity and photoperiod were controlled and were fed a diet of mice. Gastric pressures were detected by a radio telemetry transmitter (Airborne Model 430 pressure transender, Airborne Instrument Laboratories, Deer Park, NY) which was inserted into a mouse, fed to an owl therein and subsequently retrieved from the egested pellet. The transmitter was of cylindrical shape 0.8 cm in dia. and 2.5 cm in length. Prior to the initiation of experiments involving feeding of the transmitter to owls, a piece of plastic tubing with the same dimensions as the transmitter was fed to determine whether an object of this size would be harmed by, or, have any harmful affects on, the owls. The feeding of this tubing apparently did not affect the owls. Their behaviour, food intake and the nature of their excreta and pellets all appeared to be normal. * This study was partially supported by National Science Foundation Grant No. NSF-GB37254.
The transmitter transmitted at a center frequency of 2 MHz. The frequency of the transmitted signal varied in response to pressure changes exerted on the transmitter. The maximum variation of the signal was 50 kHz. The signal was received (Airborne Model 435 Receiver) and then transferred to a two-channel recorder (Hewlett-Packard Model 7402A, Hewlett-Packard, San Diego, CA) with high gain d.c. preamplifiers (HewlettPackard Model 17400A). Calibration of the transmitter, receiver and recorder was accomplished just prior to feeding the transmitter to an owl. For calibration, the transmitter was placed into a tlask in a water-bath and heated to normal body temperature of the great homed owl (39°C). Known pressures were applied to the flask causing a change in the frequency of the transmitted signal. The receiver gain was adjusted so that a given applied pressure change resulted in a predictable deflcction of the writing arm of the recorder. The owls were fed their normal diet plus the transmitter between 1500 and 1600 hours each day. The transmitted signal was recorded until a pellet containing the transmitter was egested g-20.5 hr later. Amplitudes anddurationsof contractionswereanalyzed for 1 min of every 5 min of the pressure records. The number of contractions per min (frequency) was determined from the entire 5-min period. Mean values for frequency, duration and amplitude of pressure changes were calculated for one-half hour periods and plotted on graphs for each experiment (e.g. Fig. 2). By visual inspection of each graph the data were divided into three parts representing what we theorized to be three phases of digestion. All of the data from each experiment were further assigned to one of three groups based on the quantity eaten by the owl during that experiment. Then, means for frequency duration and amplitude of pressure changes were determined for each phase of digestion for each group of experiments in which similar quantities were eaten (Table 1). 201
T. E. KOSTUCHAND G. E. DUKE
202
Table 1. Mean amplitude, frequency and duration of gastric intraluminal pressure changes during gastric digestion of three weight classes of mouse meals in great horned owls Weight class of meal (g)
No. of trials
20-40
4
90.3 (52.2)t
58.2 (38.1)
174.1 (841)
(;.:).
60-85
8
71.2 (40.9)
53.6 (78.0)
157.4 (272.1)
(G)
100+
4
Amplitude (mm Hg) I* 11* 111*
Frequency (No./min) I II III
(A::,
I
Duration (XC) II III
(Z)
23.1 (9.0)
23.7 (11.4)
19.3 (8.6)
(&
23.9 (58)
34.9 (32.5)
18.0 (9.3)
1.7 (0.4)
* The numbers I, II, III refer to three phases of gastric digestion, mechanical digestion and pellet formation and egestion. t Numbers in parentheses are standard deviations.
20-409
digestion, chemical
60-R5g I
Exp.4.0~
ICI
260 240 220 0,
200 180
E E
160 140 120 100
I
f a
,““o 40 20
.r E
‘-, 0, 3
:
t4
20 I-5 I.0 0.5 I
2 4
6
8 IO 12 I4 16 I8
2 4
6 8 IO I2 I4 16
,
,
2 4
6
I
I
I
I
I
/
L
8 IO 12 14 16 18 20
Hours
Fig. 2. Averages of amplitudes, frequencies and durations of gastric pressure changes for one-half hour periods from food ingestion to pellet egestion for three typical experiments with great homed owls. A different quantity of mice was eaten by the test owl in each experiment. C, The start of the chemical digestion phase; P, the start of the pellet formation and egestion phase. (Phases were determined by inspection of records.)
Four criteria were used for dividing data on pressure changes into three parts to designate three phases of digestion. The first phase began when food (and the transmitter) was ingested. The point at whiih amplitudes and frequencies began a major, persistent decrease and durations began a similar but opposite increase was chosen as the end of phase one and the start of phase two. The end of phase two and the start of phase three was believed to occur when amplitude and frequency each began a major, persistent increase and duration began to decrease. Pellet egestion was considered to be the end of
phase three. These points were normally apparent on the graphs from the separate experiments (e.g. Fig. 2). To study the gastroduodenal contraction sequence of the great homed owl a radiographic unit (Emperor 90/l 5 table, 6-in. image intensifier, 825 line split TV, 35 mm tine, Jupiter 90 MA control and transformer, Profexray, Des Plaines, IL) was used which consisted of components which allowed both monitoring by closed-circuit television and recording on 35 mm film (double x negative film, Type 5222, DKN 718, Eastman Kodak Co., Oak Brook, IL). Barium sulfate (Barosperse, Mallinckrodt Chemical Works, St. Louis, MO) was used as a constrast
Fig. la (upper). A series (A-E) of cineradiographic prints of a typical gastric contraction sequence in the muscular stomach of a great horned owl. The white line and arrow indicate the area undergoing contraction in each print. I, Gastric isthmus; P, pylorus; M, muscular stomach; S, small intestine; L, large intestine. Fig. I b (lower). Examples of typical intragastric pressure tracings of dicrotic (I), tricrotic (II) and biphasic (III) pressure waves. The letters A-E indicate the nature of the intragastric pressures occurring in response to contraction of each area (a+, Fig. la) of the muscular stomach. This relationship was determined by simultaneously recording intragastric pressures and radiographically observing gastric motility.
Gastric motility in great homed owls medium. It was force-fed as an aqueous suspension or it was injected into a mouse before the mouse was fed to an
owl. The presence of the telemetry transmitter during radiographic observations also aided in analysis of the gastroduodenal sequence and allowed correlation of the recorded pressure changes with the gastric contraction sequence seen radiographically. RESULTS
The pressures recorded ranged from 10 to 350 mm Hg in amplitude and averaged 943 mm Hg. Contraction frequency, throughout the recording periods, ranged from @4 to 3.0 c/min averaging 1-3 c/min. The duration of the contractions varied inversely with the frequency of contractions ranging from 5.0 to 63.0 set and averaging 24.0 sec. The wave form on the records of pressure changes was highly variable. Biphasic and triphasic, as well as dicrotic and tricrotic waves, were observed (Fig. 1). No single wave form was characteristic of any period within the record. As indicated above, when the amplitudes, frequencies and durations of pressure changes (i.e. contractions) were plotted against time, patterns which could be divided into three phases were apparent (Fig. 2). The first phase, which we have termed the phase of mechanical digestion, started immediately after eating. During this phase contraction frequency was higher than during the other two phases and averages for durations and amplitudes of contractions were intermediate to the averages for these parameters during the other two phases (Table 1). We have called the second phase the phase of chemical digestion. During this phase the contraction frequencies and amplitudes were lower and the durations were somewhat longer than during the other two phases (Table 1; Fig. 2). The third phase was called the phase of pellet formation and egestion. During this phase, the amplitude of contractions was the highest of all three phases and durations of contractions were the shortest of the three phases (Table 1; Fig. 2). In general, the average frequency of contractions during the third phase was intermediate to this average for the other two phases. During the study it became evident that the nature of gastric pressure records varied according to the
203
quantity eaten by a test owl. Thus, records were divided into three groups on the basis of quantity eaten. In general, the lengths of the three phases increased and their post-prandial starting times became later as the quantity eaten increased. As a result, the interval of time between eating and pellet egestion was also longer when a larger quantity was eaten. The mean meal-to-pellet time interval when 20-40 g were eaten was 12.8 hr (s = + 2.9). When 60-85 g were eaten this mean was 145 hr (S = + 2.5) and when 100 g or more were consumed by an owl the average meal-to-pellet interval was 185 hr (s = k2.2). Regardless of the amount eaten, amplitudes of pressure changes normally declined just prior to pellet egestion (Fig. 2). And, during the final 6-8 min prior to egestion, the amplitudes declined to less than 10 mm Hg (Table 2). The three phases of digestion were approximately equally apparent from graphs of frequency, duration and amplitude of pressure changes regardless of the quantity eaten (Fig. 2). Amplitude of contractions varied inversely with the amount eaten; however, the frequency of contractions increased with the increased amount fed. Duration of the contractions remained relatively constant regardless of the amount eaten (Fig. 2; Table 1). The gastroduodenal contraction sequence, observed primarily during phases one and two, began with a peristaltic wave of contraction moving down the glandular stomach. This was followed by a contraction sequence in the muscular stomach in which a contraction began near the isthmus and proceeded around the greater curvature of the muscular stomach to the pylorus (Fig. 1). The contraction of the duodenum began just as the contraction wave in the muscular stomach reached the pylorus. A duodenal contraction wave, as observed radiographically, rapidly moved contents throughout the duodenum. By simultaneously recording gastric pressure changes and observing gastric contractions radiographically, it was possible to correlate the development of a pressure wave with the contraction sequence of the muscular stomach. The start of the contraction sequence near the isthmus correlated with the beginning of the pressure wave. Maximum pressure was recorded during the time at which the
Table 2. Amplitudes of pressure changes recorded from the stomach or esophagus of a great homed owl during the 8nal 8 tin prior to egestion of a pellet Time prior to egestion (min) 8-7
7-6
6-5
5-4
4-3
3-2
2-1
Mean (mm Hg)
15.0
11.3
127
S.D.* (mm Hg)
14.9
N
11
11.6 7.8 13
9.9 6.2 14
8.4 6.5 14
6.9 48 13
* SD., Standard deviation.
8.9
12
7.9
13
1-O
7.2 5.3 13
T. E. KOSTUCHAND G. E.
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contraction wave was about halfway between the isthmus and pylorus. Pressure had returned to the baseline value when the contraction wave arrived at the pylorus (Fig. 1). DISCUSSION
Mangold (1911) recorded gastric pressure changes in a mouse buzzard at 05-l hr after eating. These pressure changes ranged from 8 to 20 mm Hg in amplitude and occurred at a rate of approximately 3 c/min. At a similar postprandial time, amplitudes of pressure changes reported herein averaged three to five times more than the maximum amplitude reported by Mangold. The average frequency of pressure changes was, however, less throughout the present study than the frequency reported by Mangold. In Mangold’s experiments intragastric pressures were studied by passing a balloon into the muscular stomach per OS. The mouse buzzard was restrained during the recording experiment. Perhaps these procedures inhibited the amplitude of gastric motility in the buzzard while the presence of the balloon in the birds’ stomach may have simultaneously stimulated gastric contraction frequency. On the other hand, amplitudes and frequencies of gastric pressure changes recorded by Mangold may have been unaffected by the procedures used and the mouse buzzard may indeed have had a lower amplitude and a higher frequency of gastric pressure changes than the great horned owl. Chemical digestion is apparently more thorough in hawks than in owls (Duke et al., 1975), so the amplitude of gastric pressures may be greater in owls to compensate for poorer chemical digestion. Mean amplitudes of pressure changes recorded in this study were comparable to those reported for poultry. Mean amplitudes of pressures resulting from contraction of the thick muscles of the muscular stomach in turkeys and chickens were 62 and 180 mm Hg, respectively (Duke et al., 1972). Muscles of the muscular stomach of poultry are two to three times thicker than those of the great horned owl and one might, therefore, expect to record pressure changes of greater amplitude from poultry. The gastric contraction sequence of great horned owls reported in this study and previously reported by Reed & Reed (1928) is very much different from that of turkeys (Dziuk & Duke, 1972); This difference is probably accounted for by the fact that the gross anatomy of the muscular stomach of raptors and galliforms is likewise very diss.imilar (Farner, 1960). Raptors lack the paired thick and thin muscles of the muscular stomach (Dziuk & Duke, 1972) of .galliform birds. Morever, the entire gastroduodenal contraction cycle is also different for these two groups of birds. In galliforms the thin muscles of the muscular stomach contract first in the gastroduodenal contraction sequence, then the
DUKE
duodenum, next the thick muscles of the muscular stomach and lastly the glandular stomach (Nolf, 1938a, b; Dziuk &Duke, 1972). The gastroduodenal contraction sequence described herein for owls has not been previously detailed for raptors. These anatomical and functional differences between raptors and galliforms are apparently related to their different food habits. Since amplitudes of pressures occurring in the muscular stomach of great horned owls and poultry are similar, the contraction pattern of the muscular stomach must be more important in mechanical digestion than the pressure generated by muscular stomach contractions. Apparently the gastric contraction sequence in fowl is more appropriate for grinding grain than the more simple sequence seen in the muscular stomach of the owl. Distinct phases in the digestion of a meal have not been previously reported for birds. In addition, reports of long-term recording of gastric motility in birds, as described herein, could not be found. The four phases in rumination (Phillipson, 1970) and the filling, mechanical digestion and emptying phenomena in the gastric digestion of a meal in mammals with simple stomachs (Hightower, 1966) are not comparable to the phases described herein. As the names selected for the three phases described herein suggest, these phases in gastric motility probably represent stages in the gastric digestion of a meal. It is hypothesized that food is primarily crushed and macerated and then mixed with gastric secretions during the first, or mechanical digestion phase. During the second, or chemical digestion phase, low-amplitude contractions probably gently mix ingesta with gastric digestive secretions. A great deal of gastric digestion probably occurs during this phase. It is likely that soft tissues are digested from bones and broken into very small particles which can be emptied from the muscular stomach during the second phase, but it is doubtful that much ingesta is emptied at that time. During the phase of pellet formation and egestion, fluid ingesta are probably emptied from the stomach by the high amplitude contractions characteristic of that phase. These contractions probably also compact the remaining hair and bones into a pellet. It is possible that the process of pellet egestion is more comparable to regurgitation than to emesis. Pressures recorded during the last few minutes prior to egestion are very low in amplitude which would indicate that the high amplitude intragastric pressures characteristic of emesis (Hightower, 1966) were not occurring. Regurgitation of ingesta as a normal regularly recurring physiological process is characteristic of ruminants (Anderson & Jones, 1967) but apparently ,does not .occur normally in other mammals. Lengths of the three phases observed in this investigation, overa& meaLto-pellet interval and post-prandial starting time of each phase varied with
Gastric motility in great homed owls the quantity eaten. This variation was apparent from graphs of either frequency, duration or amplitude of gastric pressure changes. Therefore, if one could transmit information on gastric motility in a free-living great horned owl, using long-range radiotelemetry, the amount eaten by the owl could be estimated. Pellet egestion should be detected by this system also. By pinpointing the position of the owl at the time of egestion, many pellets could be collected and the nature of the meal responsible for the pellet could be determined. This system would provide valuable information on energetics of great horned owls. SUMMABY Gastric motility was studied in four great horned owls by intragastric pressure telemetry and by radiographic observation. Amplitudes, frequencies and durations of gastric pressure changes averaged 94.3 mm Hg, 1.3 c/mm and 24.0 set, respectively. Amplitudes, frequencies and durations of gastric pressure changes varied during the gastric digestion of a meal in such a way that three successive phases of gastric digestion were apparent from pressure records. These phases were called the mechanical digestion phase, chemical digestion phase and pellet formation and egestion phase. Contraction frequency was greatest during the first phase while contraction amplitude was greatest during the third phase. Lengths of the phases and overall meal-topellet time interval increased as the quantity eaten by an owl increased. The gastroduodenal contraction sequence was observed radiographically to begin in the glandular stomach. Contractions then proceeded into and through the muscular stomach and finally on into the duodenum. In the muscular stomach the contraction cycle began adjacent to the gastric isthmus and proceeded around the circumference of the muscular stomach to the pylorus.
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staff at the Veteran’s Administration Hospital, Mirmeapolis, Minnesota, particularly Dr. U. S. Seal, Mrs. D. Gaiser and Mr. T. Stoebe, in making cineradiographic equipment available to us was greatly appreciated. We are very grateful to Mr. Jerry Schlegel of the Mayo Clinic, Rochester, Minnesota, for the temporary loan of a telemetry transmitter which enabled us to fmish our study. REFERENCES
ANDERSON S. & JONESJ. K., JR. (1967) Recent Mammals ofthe World, p. 402. Ronald Press, New York. DUKE G. E., Dzrurc H. E. & EVANXIN0. A. (1972) Gastric pressure and smooth muscle electrical potential changes in turkeys. Am.J. Physiol. 222,167-173. DUKE G. E., JEGERSA. A., LOFFG. & EVAN.WN0. A. (1975) Gastric digestion in some raptors. Comp. Biochem. Physiol. (In preparation.) Dzru~ H. E. & DUKE G. E. (1972) Cineradiographic studies of gastric motility in turkeys. Am. J. Physiol. 222,159-166. FARNERD.
S. (1960) The digestive system and digestion. In Biology and Comparative Physiology of Birds (Edited by MARSHALLA. J.), Vol. I, pp. 411-467. Academic Press, New York. HIGHTOWERN. C. (1966) Movements of the alimentary canal. In The Physiological Basis of Medical Practice (Edited by BELTC. H. & TAYLORN. B.), 8th Edn., pp. 1196-1241. Williams &Wilkins, Baltimore. MANGOLDE. (1911) Die funktionellen Schwankungen der motor&hen Tatigkeit des Raubvogelmagens. Ppiger ‘s Arch. ges. Physiol. 139,10-32. NOLF
P. (1938a) L’appareil nerveux de l’automatisme gastrique de l’oiseau-I. Essai d’analyse par la nicotine. Archs int. Physiol. 46,1-85. NOLF P. (1938b) L’aonareil nerveux de l’automatisme gastriquk de Boise&-II. Etude des effets causes par une ou plusieurs sections de l’anneau nerveux du gesier. Archs int. Physiol. 46,441-559. PHILLIPSON A.
T. (1970) Ruminant digestion. In Dukes’ Physiology of Domestic Animals (Edited by SWENWN
M. J.), 8th Edn., pp. 424483. Cornell University Press, Ithaca. REEDC. I. & REEDB. P. (1928) The mechanism of pellet formation in the great homed owl (Babe virginianus). Science, Wash. 68,359-360.
authors are grateful for technical assistance from Miss A. A. Jegers and Mr. D. D. Rhoades throughout the study. The help of the research Acknowledgements-The
Key Word Index-Raptor; motility; gastric motility.
owl; owl digestion; GI