- Email: [email protected]
Regulation of pellet egestion: The effects of multiple feedings on meal to pellet intervals in great horned owls
Corn,, Bh,chrm Phrwl.. 0 Puy”mo” PW\.S Lid
0300-9621)
Vol. 62A. pp. 439 IO 444 1979. Pr,ntrd I,, Grvur Blwub,
79 ON-,,43YS,EoO;O
REGULATION OF PELLET EGESTION: THE EFFECTS OF MULTIPLE FEEDINGS ON MEAL TO PELLET INTERVALS IN GREAT HORNED OWLS MARK R. FULLER and GARY E. DUKE Department of Veterinary Biology, College of Veterinary Medicine, University of Minnesota, 1988 Fitch Avenue, St. Paul, MN 55108. U.S.A. (Rewired
14 March 1978)
Owls fed a meal of mice, divided into two or three equal portions and fed over a period of time, had a longer meal to pellet interval (MPI) than when a similar sized meal was ingested as one portion. 2. Two of four owls occasionally egested a pellet after each portion of a meal fed at 1900 and 0700 hr on successive days, and the combined time of the two MPIs was always less than the MPI resulting from a single pellet egested after both portions of a similar sized meal had been ingested. 3. The ingestion of one or two portions of a meal at intervals after ingestion of the initial portion partially interrupts gastric digestion of the initial portion. When multiple feedings were separated by sufficient time to permit digestion of the first portion to reach “Late Pellet Compaction” phase (Rhoades and Duke, Condor, 79. 328-334, 1977). a pellet was egested before the second portion was ingested. Abstract-l.
deep) using standard falconry techniques. Personnel access to the room was limited to the feeding periods (see below). The owls were acclimated to these housing conditions and fed a single meal of mice for IO days before data collection was initiated. The owls were in good health and had been fed ad libitum for several weeks so they had achieved a stable body weight prior to the experiments. The experiments were conducted from January to April. Any physiological changes due to annual cycles were not believed to have significantly affected the results. The standard diet for experiments was laboratory mice (Mus musculus), which were fresh or thawed from fresh frozen supplies. The total amount fed daily consisted of two or three mice weighing [email protected] g in foto [mice average 37.8% dry matter (DM); Duke et al. (1975)]. This quantity was presented in one, two or three approximately equal portions. All uneaten remains were removed and weighed after a 30-min feeding period and the total meal size recorded. The owls were fed on the following schedules :
INTRODUCTION The mechanisms of pellet formation (Grimm & Whitehouse, 1963; Duke et al., 1976~) and egestion in owls (Duke et a!., 1976~) have been fairly well characterized. Factors regulating the timing of these events within the digestion process are, however, less well understood. For owls it has been shown that the quantity ingested (Smith & Richmond, 1972; Duke et al., 1976a) and amounts of proteinaceous, lipid and “fibrous” material in the meal (Duke & Rhoades, 1977) may affect the meal to pellet interval (MPI). Only one factor has been found which appears to have a major influence on the time of egestion by hawks, viz. “lights-on” (dawn) in the laboratory (Balgooyen, 1971; Duke et al., 1976a). In most previous studies a daily meal was offered to raptors for a limited time once each day. Few studies have been conducted to test the effects of natural feeding patterns on the length of a raptor’s MPI. However, observations on one short-eared owl (Asia jkmmeus), by Chitty (1938), and one barn owl (Tyto &a) by Smith & Richmond (1972) suggested that multiple feedings may increase the MPI. The objectives of the experiments reported herein were to describe and quantify the effects of multiple feedings on the regulation of digestion and pellet egestion in great-horned owls (Bubo virginianus).
Experiment 1 2 3 4
no.
Feeding
time
1700 1700, 1930.2200 1700,220O 1900,0700
Number of days fed at this time 20 30 31 I6
The results from Experiment 4 provided instances when owls egested one pellet after both portions had been fed. and instances when one pellet was egested after each protion was fed. The results of the former will be referred to as 4a and the latter as 4b. The MPI for all experiments was measured from the time the first portion was ingested until pellet egestion. Pellet egestion was monitored with automatic timing devices in which egested pellets were directed, via a sloping chute under each owl, to a wire mesh basket. The addition of a small (0.5 g) weight (e.g. pellet) to this basket closed a microswitch activating a circuit which caused a pen to mark paper on a drum which rotated at a constant known speed. Sample sizes were smaller than they would have
METHODS Four 5-yr old great-horned owls were used to measure MPIs. These birds had been held in the lab since they were nestlings and were very tractable and accustomed to our experimental conditions. Experiments were performed in environmentally controlled rooms in which temperature was maintained between 21_23”C, relative humidity was kept between 40 and 50% and the photoperiod was automatically timed to provide 14 hr of light from 0700 to 2100 hr. The owls were jessed and kept on perches in individual chambers (240 cm high, 125 cm wide and l20cm 439
been if data from each brrd were a\ailnbie ever) day the experiment was corducted because pellets did not always reach the basket. owls did not cat all of their meal. or the microswitches were erroneously “rripped” by feathers. etc. The MPls for each bird were combined to provide data for determination of a mean. range and standard deviation. The variance of results from each experiment was tested by the I,‘-test. and if signlticantly different. means of these experiments were tested using the Flsher~-Behrens test. Experiments with similar 1 ariancea were compared using Stu-
stomach of a barred out (.S~rr.\ rcrrrl pre\11ou\ly zmplantcd for use In another study. The oul \~;ts fed on .t \rmilar schedule to that used with the great-horned owls In feeding Experiments I, 2 and 3 (above). Trchniqucc TOI-obtutnlng motility data from chronlcallq Implanted extralumlnal SGT have been described previously (Duke CI
dent’s r-tclrt of means (Rickmers & Todd. IO). Six pcrmancntly crippled great-horned owls w&e fed 011
HESLLTS
the same schedules used in cupcrimcnts I 4. above. To faciiitatc ~de~~t~fi~ation of each portion of their meals. different colored mice wcrc fed. and birds wcru sacrificed at the following times:
The mean (four owls) MPI from meals consumed as one portion at 1700tlr (Experiment 1) was significantly shorter than the means for those meals eonsumed in three portions given at 2.5 hr intervals (Experiment 2) or those eaten in two portions fed 5 hr apart (Experiment 3) (Table I). The mean MPI of the meals fed in two portions, 5 hr apart was longer than that of meals fed in three portions over a period of 5 hr. but this difference was not StatisticalIy significant. When two portions of a meat were fed at a 12 hr interval. pellets were occasionnlly egested by two of the owls before the second portion was presented to them. However. on most occasions, owls fed 1.5 mice at 191x)hr, and another 1.5 mice I :! hr later (0700 hr) ogcsted only one pcltet after the second portion of the meal (Table 1). According to the Fisher Behrens test. the mean MPI from experiment 4a was significantly longer than those of experiments I. 2 and 3. The mean of 14 MPIs recorded when owls I and 4 egested pellets after both the t900 and 0700 hr feedings (Experiment 4b) was 9.27 hr (Table l), which was significantly less than the MPI from one large meal fed at 1700 hr. Portions of meals resulting in a pellet
__~.__ Experiment __.---.--~
Feeding time (set)
no.
I
Sacriticc
1700 17(X). I9iO. 2200 1700 I 700. 2200
3
3
1900
4
IWO. 0700
_.-
lime
lo00
x30 2900 0 too 0700
IO00
lmmed~ately after euthanasia (3.Ocm” sodium pentabarbitol. IV). gastrointestinal lGI) tracts of the owls were removed. The contents of the proventriculus. ventriculus and duodenum were visually analysed and compared to determine the extent of digestion, volume of contents of each organ, and amount of moisture in the contents under the various feeding schedules. The influence of multiple feedings on patterns of gastric motility were assessed by recording gastric motility via a semi-conductor strain gauge transducer (SGT) chronically implanted on the caudoventral surface of the muscular
Table
I. Meal to pellet
intervals
(MPI)
obtained
on a diet of mice using four feeding schedules Feeding
Exp. I I 700 hl
Exp. 2 1700 hr 1930 hr 1200 hr
2
x
‘0.74
S.D.
& 1.01
; SD.
3
; S.D.
4
great-horned
owls fed according
to
schedules Exp. 3 I700 hr 200 hr
E:xp. Ja 1900 hl 0700 hr I pellet produced
Exp. 4b 1900 hr 0700 hr 7 pellet> produced
MPI (hr)
OWI
I
four
;; SD.
13 19.X8 iO.X3 24 19.95 i 1.18 14 19.95 I I .h2
70 OvZrall X s. D. II
20.63 + 1.41 F,,, 91
* Tz,3,p,, indicates a significant difference between the mean t F,, indicates a significant difference between the variances test. I = 0.05).
10.2 * 0.5
s
X.76 + 7.29 _ 0 9.27 i_
i .Y6 14
of Exp. I and 2. 3. 4b etc. (Student’s t-test. r = 0.5) of Elcp. I and 4a (F-test) and means (Fischer-Behrens
Regulation
of pellet egestion
Table 2. Number of meals which, when fed in two portions at 1900 and 0700 hr resulted in either one pellet for both portions or two pellets per day, one for each portion Weight
(g D.M.) of meals fed in two portions at 1900 and 0700 hr lCk-15 16-20 2 I --2.5 26-30
No. of meals* yielding I pellet No. of meals yielding 2 pellets
Total no. of pellets
2
9
25
I1
47
0
I
4
3
14t
* Each meal was fed in two portions in this experiment. t On two occasions pellets were cast but the casting time was not recorded.
about 9.3 hr either a 1900 or 0700 hr feeding averaged 11.2 g D.M. which is within the range of meal sizes of meals which resulted in only one pellet after both the 1900 and 0700 hr feedings, i.e. a smaller than normal meal size apparently was not the only stimulus for egestion of two pellets per day in experiment 4 (Table 2). The sum of the two MPIs for the two pellet egestions associated with the 1900 and 0700 hr feedings of a meal was always less than the one MPI resulting from egestion of one pellet after ingestion of both the 1900 and 0700 hr portions of a meal of similar size (Table 1). When the barred owl was fed a meal in one portion at 1700 hr (n = 19) the frequency of gastric contractions increased from the pre-prandial mean of 1.09 f 0.33/min to 1.67 f 0.49/min. This increase in contractility occurred within an average of O-7 min of ingestion, then frequency decreased to a mean level of 0.97 * O.l9/min which was maintained for 2-6 hr (dependmg upon the quantity ingested). Following this period of reduced contractile activity the frequency of contraction gradually increased to a maximum of to 2.5-3.0 contractions/min at the time of egestion (Fig. la). When this barred owl ingested a meal in two portions, 5.0 hr apart (n = 3) or three portions, 2.5 hr apart (n = 6), the pattern of motility observed during the digestion of one-portion meals was “interrupted” by the ingestion of each new portion. Each time the barred owl ingested a second or third portion, the rate of contraction reverted from that of moderate frequency of about 1 contraction/min to a higher frequency most similar to that characteristic of the immediate post-prandial period (Fig. lb). The time elapsing between ingestion of the second or third portion and renewed high frequency contractions was from 0 to 10.5min. The subsequent period of increased motility lasted 1680 min, until the moderate motility of about 1 contraction/min was resumed. When an owl fed one mouse at 1700 hr was euthanized 3 hr later, the gastric digesta consisted of a bolus composed primarily of small, firm balls of fine fur, loose coarse hair and bone. The bolus was sufficiently compact that it retained its shape after removal from the gizzard, and, although it was damp, moisture could not be squeezed from it. Only fragments of tissue from the larger muscle masses of the limbs remained; the tail was intact although little soft within
tissue could be detected visually. In the second sacrifice experiment, an owl was fed a total of three mice (a black one, then white, then black) at 2.5 hr intervals and sacrificed 0.5 hr after the last mouse was eaten. The first mouse ingested was completely digested within this 5.5 hr period. Digestion of the second mouse, ingested 3 hr before sacrifice, had not proceeded nearly as far in 3 hr as had digestion of the mouse fed as a “single-mouse meal” to the first owl sacrificed. The hind limbs were still attached to the pelvic girdle, muscle tissue remained on the bones, and neural tissue remained in the skull. The third mouse, at only 0.5 hr after ingestion, was intact and was resting at the cranial end of a rather wet bolus of gastric digestia from which fluid could be squeezed. In the third sacrifice experiment, a moist nearly formed pellet was found in the gizzard of an owl sacrificed 5 hr after having eaten 1.5 mice. Using a fourth owl, three mice were fed in two portions 5.0 hr apart and the owl was sacrificed 3 hr after the second por-
Time of day Fig. I. Frequencies of gastric contractions (detected by gastric extraluminal strain-gauge transducers) in a barred owl plotted by IOmin periods from food (mice) ingestion to pellet egestion for a meal eaten in one portion (A) or in three portions at I hr intervals (B). Interruptions in the plot indicate a failure to record data for a brief period usually due to technical difficulties.
t~on was eaten. The second portion was only partly digested after undergoing 3.0 hr of gastric digestion. Its appearance was similar to that of the second mouse ingested by the second sacrificed owl (above). When a fifth owl was sacrificed 12.0 hr after eating I.5 mice. a damp well-formed pellet of fur and bones was found in its gizzard. The last owl was fed 1.5 mice at 1900 hr. I.5 mice at 0700 hr. and sacrificed at 1000 hr. The I.5 mice making up the second portion of this meal were still almost completely articulated and were only minimally digested. The well digested remains of the first I.5 mouse-portion of the meal were interspersed with the second portion.
We found, as Chitty (3938) and Smith & Richmond (1972) had suggested. that the length of time required to digest food and egest a pellet increases when the daily food intake of an owl consists of several portions ingested over a period of time rather than all at once. Data obtained from our experiments more accurately reflect the ingestion schedule of wild owls and therefore their MPIs. The analyses of ingesta and recordings of gastric motility at various intervals after multiple feedings provide a more complete understanding of the influence of multiple daily feedings on the regulation of digestion. Patterns of gastric motility obtained via the extraluminal SGT in a barred owl were like those described previously for owls fed under similar conditions (Kostuch & Duke, 1975; Rhoades & Duke. 1978). As the barred owl swallowed food gastric motility increased during the “Filling Phase” (Phase 1). then decreased to a level maintained during “Early Chemical Digestion” (Phase II). and late ‘*Chemical Digestion” (Phase III) (Rhoades & Duke, 1978). The frequency of contractions gradually increased through “Early Pellet Compaction” (Phase IV) and “Late Pellet Compaction” (Phase V) until the maximum frequency of contractions was reached just prior to pellet egestion (Rhoades & Duke, 1978). When the barred owl was fed a second or third portion of its daily meal at 2.5 or 5 hr intervals, during Phase II, the motility reverted to Phase I within a few minutes. This renewed “Filling Phase” lasted about 0.25 I .SOhr, after which motility representative of chemical digestion resumed. Each time food was ingested after a previous portion had been partially digested. gastric motility was interrupted. it reverted to the filling stage. then resumed contraction patterns characteristic of chemical digestion. This delay in the digestive sequence was apparently partly responsible for the longer MPIs recorded from multiple feedings. While the motility pattern remained relatively constant through chemical digestion if not interrupted, the appearance of the ingesta in the ventriculus changed dramatically. Those three instances in which the contents of the GI tract of an owl were examined before a second portion was ingested allowed us to ascertain the phase of digestion (Rhoades & Duke, 1978) which had been reached. Three hours after ingestion of one mouse “Late Chemical Digestion” (Phase III) (Rhoades & Duke, 1978) was underway. When the ingesta were analyzed 30 min after the third of three portions fed at 2.5 hr intervals had been in-
gested (Sacrifice Experiment 2) the first mouse was found to have been thoroughly digested. but rhe second mouse. which had been in the
Regulation
of pellet egestion
tion with a second portion and apparently even more efficiently than if it had ingested the entire meal at one time. As several investigators have pointed out, the smaller the quantity ingested by an owl, the shorter the MPI (see Kostuch & Duke, 1975; Duke & Rhoades, 1977). The range of meal sizes fed in experiment 4 (Table 2) which produced two pellets in one 24 hr period, suggests that additional factors also influence MPI because both small and large meals resulted in two pellets/day. The size of the meal fed the previous day and thus the level of hunger of the owl is probably an additional factor affecting rates of digestion. Since only two of the four owls cast two pellets under this schedule individual variability may also be involved. Additionally, we have observed that an owl allowed to see food near the end of its expected MPI may egest a pellet earlier than expected. Perhaps the two owls which egested two pellets per day “anticipated” the second portion thus hastening the onset of pellet egestion. Whatever the cause of instances resulting in more rapid digestion of the first portion of the meal, the effect was a reduced time for the total daily ration. Fuller (1978) found that the natural activity patterns of free-ranging great-horned owls and barred owls often exhibited two peaks of activity, one beginning just before sunset and ending before midnight and another beginning about 0300 hr and ending near sunrise. This biphasic activity pattern is not uncommon among nocturnal animals (Aschoff, 1966). If an owl begins hunting soon after the onset of evening activity it may capture and ingest part of its daily nutritional requirements. Depending on the size of the portion ingested the owl may or may not egest a pellet before ingesting prey on the next morning. Egestion of a pellet from the evening meal would allow ingestion of a larger meal the next morning. The meal could be larger both relative to what might have been eaten if a pellet were not egested before eating and also relative to what was eaten on the previous evening. Eating a larger meal at sunrise than at dusk might be preferable since MPI for meals eaten at dawn was found to be shorter than for meals eaten in late afternoon (Duke & Rhoades, 1977) so a large meal at dawn might still be digested rapidly enough to permit pellet egestion before the evening hunt. Data of this nature provide a better understanding of factors affecting the regulation of digestion and they are valuable for strengthening models t!lat attempt to predict the most efficient predatory and bioenergetic strategies (e.g. Schoener, 1971). The data may also be applied to studies of owl food habits in which knowledge of the production of more than one pellet per day and MPI are essential for proper interpretation and quantification of food habits data (Howard, 1958; Marti, 1973).
443
Acknowledgements-We wish to thank J. E. Miller and P. S. Foxworthy for assistance during this study, and acknowledge support from NSF Grant GB 37254.
REFERENCES ASCHOFF J. (1966) Circadian activity pattern with two peaks. Ecology 41, 1657-1662. BALGWTEN T. G. (1971) Pellet regurgitation by captive sparrow hawks (F&o sparcerius). Condor 73, 382-385. CHATTYD. (1938) Pellet formation in short-eared owls, Asio ,jammeus. Proc. zool. Sot. Lond. A, 108,261-287. DUKE G. E., EVANSON 0. A. & JEGERS A. A. (1976a) Meal to pellet intervals in 14 species of captive raptors. Comp. Biochem. Physiol. 53A, l-6. DUKE G. E., EVANSON 0. A. & REDIG P. T. (1976b) A cephalic influence on gastric motility upon seeing food in domestic turkeys (Melagris gallopaoo), great-horned owls (Bubo virginianus) and red-tailed Hawks (Buteo jamaicensis). Poultry Sci. 55, 2155-2165. DUKE G. E.. EVANSON 0. A., REDIG P. T. & RHOADES D. D. (1976~) The mechanism of pellet egestion in greathorned owls. Am. J. Physiol. 231. 1824-1829. DUKE G. E., JEGERS A. A., LOFF G. & EVANSON 0. A. (1975) Gastric digestion in some raptors. Camp. Biochem. Physiol. 50A,649-656. DUKE G. E. & RHOADES D. D. (1977) Factors affecting meal to pellet intervals in great-horned owls (Bubo cirginianus). Camp. Biochem. Physiol. %A. 283-286. EARHART C. M. & JOHNSON N. K. (1970) Size dimorphism and food habits of North American owls. Condor 72, 251-264. ERRINGTON P. L. (1930) The pellet analysis method of raptor food habits study. Condor 32, 292-296. ERRINGTON P. L. (1932) Techniques of raptor food habits study. Condor 34, 75-86. FULLER M. R. (1978) Spatial temporal ecology of four species of sympatric raptors. Ph.D. dissertation, University of Minnesota. GRIMM R. 1. & WHITEHOUSE W. M. (1963) Pellet formation in great-horned owl: a roentgenographic study. Auk 80, 301-306. HOWARD W. E. (1958) Food intake and pellet formation of a horned owl. Wilson Bull. 70, 145-150. KOSTUCH T. E. & DUKE G. E. (1975) Gastric motility in great-horned owls (Bubo virginianus). Comp. Biochem. Physiol. 51A,201-205. MARTI C. D. (1974) Feeding ecology of four sympatric owls. Condor 76, 45-61. RHOADES D. D. & DUKE G. E. (1978) Cineradiographic studies of gastric motility in the great-horned owl. Condor 79, 328-334. RICKMERS A. D. & TODD H. N. (1969) Statistics, 585 pp. McGraw-Hill, New York. SCHOENER T. W. (1971) Theory of feeding strategies. A. Rec. Ecol. Syst. 369404. SMITH C. R. & RICHMOND M. E. (1972) Factors influencing pellet egestion and gastric pH in the barn owl. Wilson Bull. 84, 179-186.
0300-9621)
Vol. 62A. pp. 439 IO 444 1979. Pr,ntrd I,, Grvur Blwub,
79 ON-,,43YS,EoO;O
REGULATION OF PELLET EGESTION: THE EFFECTS OF MULTIPLE FEEDINGS ON MEAL TO PELLET INTERVALS IN GREAT HORNED OWLS MARK R. FULLER and GARY E. DUKE Department of Veterinary Biology, College of Veterinary Medicine, University of Minnesota, 1988 Fitch Avenue, St. Paul, MN 55108. U.S.A. (Rewired
14 March 1978)
Owls fed a meal of mice, divided into two or three equal portions and fed over a period of time, had a longer meal to pellet interval (MPI) than when a similar sized meal was ingested as one portion. 2. Two of four owls occasionally egested a pellet after each portion of a meal fed at 1900 and 0700 hr on successive days, and the combined time of the two MPIs was always less than the MPI resulting from a single pellet egested after both portions of a similar sized meal had been ingested. 3. The ingestion of one or two portions of a meal at intervals after ingestion of the initial portion partially interrupts gastric digestion of the initial portion. When multiple feedings were separated by sufficient time to permit digestion of the first portion to reach “Late Pellet Compaction” phase (Rhoades and Duke, Condor, 79. 328-334, 1977). a pellet was egested before the second portion was ingested. Abstract-l.
deep) using standard falconry techniques. Personnel access to the room was limited to the feeding periods (see below). The owls were acclimated to these housing conditions and fed a single meal of mice for IO days before data collection was initiated. The owls were in good health and had been fed ad libitum for several weeks so they had achieved a stable body weight prior to the experiments. The experiments were conducted from January to April. Any physiological changes due to annual cycles were not believed to have significantly affected the results. The standard diet for experiments was laboratory mice (Mus musculus), which were fresh or thawed from fresh frozen supplies. The total amount fed daily consisted of two or three mice weighing [email protected] g in foto [mice average 37.8% dry matter (DM); Duke et al. (1975)]. This quantity was presented in one, two or three approximately equal portions. All uneaten remains were removed and weighed after a 30-min feeding period and the total meal size recorded. The owls were fed on the following schedules :
INTRODUCTION The mechanisms of pellet formation (Grimm & Whitehouse, 1963; Duke et al., 1976~) and egestion in owls (Duke et a!., 1976~) have been fairly well characterized. Factors regulating the timing of these events within the digestion process are, however, less well understood. For owls it has been shown that the quantity ingested (Smith & Richmond, 1972; Duke et al., 1976a) and amounts of proteinaceous, lipid and “fibrous” material in the meal (Duke & Rhoades, 1977) may affect the meal to pellet interval (MPI). Only one factor has been found which appears to have a major influence on the time of egestion by hawks, viz. “lights-on” (dawn) in the laboratory (Balgooyen, 1971; Duke et al., 1976a). In most previous studies a daily meal was offered to raptors for a limited time once each day. Few studies have been conducted to test the effects of natural feeding patterns on the length of a raptor’s MPI. However, observations on one short-eared owl (Asia jkmmeus), by Chitty (1938), and one barn owl (Tyto &a) by Smith & Richmond (1972) suggested that multiple feedings may increase the MPI. The objectives of the experiments reported herein were to describe and quantify the effects of multiple feedings on the regulation of digestion and pellet egestion in great-horned owls (Bubo virginianus).
Experiment 1 2 3 4
no.
Feeding
time
1700 1700, 1930.2200 1700,220O 1900,0700
Number of days fed at this time 20 30 31 I6
The results from Experiment 4 provided instances when owls egested one pellet after both portions had been fed. and instances when one pellet was egested after each protion was fed. The results of the former will be referred to as 4a and the latter as 4b. The MPI for all experiments was measured from the time the first portion was ingested until pellet egestion. Pellet egestion was monitored with automatic timing devices in which egested pellets were directed, via a sloping chute under each owl, to a wire mesh basket. The addition of a small (0.5 g) weight (e.g. pellet) to this basket closed a microswitch activating a circuit which caused a pen to mark paper on a drum which rotated at a constant known speed. Sample sizes were smaller than they would have
METHODS Four 5-yr old great-horned owls were used to measure MPIs. These birds had been held in the lab since they were nestlings and were very tractable and accustomed to our experimental conditions. Experiments were performed in environmentally controlled rooms in which temperature was maintained between 21_23”C, relative humidity was kept between 40 and 50% and the photoperiod was automatically timed to provide 14 hr of light from 0700 to 2100 hr. The owls were jessed and kept on perches in individual chambers (240 cm high, 125 cm wide and l20cm 439
been if data from each brrd were a\ailnbie ever) day the experiment was corducted because pellets did not always reach the basket. owls did not cat all of their meal. or the microswitches were erroneously “rripped” by feathers. etc. The MPls for each bird were combined to provide data for determination of a mean. range and standard deviation. The variance of results from each experiment was tested by the I,‘-test. and if signlticantly different. means of these experiments were tested using the Flsher~-Behrens test. Experiments with similar 1 ariancea were compared using Stu-
stomach of a barred out (.S~rr.\ rcrrrl pre\11ou\ly zmplantcd for use In another study. The oul \~;ts fed on .t \rmilar schedule to that used with the great-horned owls In feeding Experiments I, 2 and 3 (above). Trchniqucc TOI-obtutnlng motility data from chronlcallq Implanted extralumlnal SGT have been described previously (Duke CI
dent’s r-tclrt of means (Rickmers & Todd. IO). Six pcrmancntly crippled great-horned owls w&e fed 011
HESLLTS
the same schedules used in cupcrimcnts I 4. above. To faciiitatc ~de~~t~fi~ation of each portion of their meals. different colored mice wcrc fed. and birds wcru sacrificed at the following times:
The mean (four owls) MPI from meals consumed as one portion at 1700tlr (Experiment 1) was significantly shorter than the means for those meals eonsumed in three portions given at 2.5 hr intervals (Experiment 2) or those eaten in two portions fed 5 hr apart (Experiment 3) (Table I). The mean MPI of the meals fed in two portions, 5 hr apart was longer than that of meals fed in three portions over a period of 5 hr. but this difference was not StatisticalIy significant. When two portions of a meat were fed at a 12 hr interval. pellets were occasionnlly egested by two of the owls before the second portion was presented to them. However. on most occasions, owls fed 1.5 mice at 191x)hr, and another 1.5 mice I :! hr later (0700 hr) ogcsted only one pcltet after the second portion of the meal (Table 1). According to the Fisher Behrens test. the mean MPI from experiment 4a was significantly longer than those of experiments I. 2 and 3. The mean of 14 MPIs recorded when owls I and 4 egested pellets after both the t900 and 0700 hr feedings (Experiment 4b) was 9.27 hr (Table l), which was significantly less than the MPI from one large meal fed at 1700 hr. Portions of meals resulting in a pellet
__~.__ Experiment __.---.--~
Feeding time (set)
no.
I
Sacriticc
1700 17(X). I9iO. 2200 1700 I 700. 2200
3
3
1900
4
IWO. 0700
_.-
lime
lo00
x30 2900 0 too 0700
IO00
lmmed~ately after euthanasia (3.Ocm” sodium pentabarbitol. IV). gastrointestinal lGI) tracts of the owls were removed. The contents of the proventriculus. ventriculus and duodenum were visually analysed and compared to determine the extent of digestion, volume of contents of each organ, and amount of moisture in the contents under the various feeding schedules. The influence of multiple feedings on patterns of gastric motility were assessed by recording gastric motility via a semi-conductor strain gauge transducer (SGT) chronically implanted on the caudoventral surface of the muscular
Table
I. Meal to pellet
intervals
(MPI)
obtained
on a diet of mice using four feeding schedules Feeding
Exp. I I 700 hl
Exp. 2 1700 hr 1930 hr 1200 hr
2
x
‘0.74
S.D.
& 1.01
; SD.
3
; S.D.
4
great-horned
owls fed according
to
schedules Exp. 3 I700 hr 200 hr
E:xp. Ja 1900 hl 0700 hr I pellet produced
Exp. 4b 1900 hr 0700 hr 7 pellet> produced
MPI (hr)
OWI
I
four
;; SD.
13 19.X8 iO.X3 24 19.95 i 1.18 14 19.95 I I .h2
70 OvZrall X s. D. II
20.63 + 1.41 F,,, 91
* Tz,3,p,, indicates a significant difference between the mean t F,, indicates a significant difference between the variances test. I = 0.05).
10.2 * 0.5
s
X.76 + 7.29 _ 0 9.27 i_
i .Y6 14
of Exp. I and 2. 3. 4b etc. (Student’s t-test. r = 0.5) of Elcp. I and 4a (F-test) and means (Fischer-Behrens
Regulation
of pellet egestion
Table 2. Number of meals which, when fed in two portions at 1900 and 0700 hr resulted in either one pellet for both portions or two pellets per day, one for each portion Weight
(g D.M.) of meals fed in two portions at 1900 and 0700 hr lCk-15 16-20 2 I --2.5 26-30
No. of meals* yielding I pellet No. of meals yielding 2 pellets
Total no. of pellets
2
9
25
I1
47
0
I
4
3
14t
* Each meal was fed in two portions in this experiment. t On two occasions pellets were cast but the casting time was not recorded.
about 9.3 hr either a 1900 or 0700 hr feeding averaged 11.2 g D.M. which is within the range of meal sizes of meals which resulted in only one pellet after both the 1900 and 0700 hr feedings, i.e. a smaller than normal meal size apparently was not the only stimulus for egestion of two pellets per day in experiment 4 (Table 2). The sum of the two MPIs for the two pellet egestions associated with the 1900 and 0700 hr feedings of a meal was always less than the one MPI resulting from egestion of one pellet after ingestion of both the 1900 and 0700 hr portions of a meal of similar size (Table 1). When the barred owl was fed a meal in one portion at 1700 hr (n = 19) the frequency of gastric contractions increased from the pre-prandial mean of 1.09 f 0.33/min to 1.67 f 0.49/min. This increase in contractility occurred within an average of O-7 min of ingestion, then frequency decreased to a mean level of 0.97 * O.l9/min which was maintained for 2-6 hr (dependmg upon the quantity ingested). Following this period of reduced contractile activity the frequency of contraction gradually increased to a maximum of to 2.5-3.0 contractions/min at the time of egestion (Fig. la). When this barred owl ingested a meal in two portions, 5.0 hr apart (n = 3) or three portions, 2.5 hr apart (n = 6), the pattern of motility observed during the digestion of one-portion meals was “interrupted” by the ingestion of each new portion. Each time the barred owl ingested a second or third portion, the rate of contraction reverted from that of moderate frequency of about 1 contraction/min to a higher frequency most similar to that characteristic of the immediate post-prandial period (Fig. lb). The time elapsing between ingestion of the second or third portion and renewed high frequency contractions was from 0 to 10.5min. The subsequent period of increased motility lasted 1680 min, until the moderate motility of about 1 contraction/min was resumed. When an owl fed one mouse at 1700 hr was euthanized 3 hr later, the gastric digesta consisted of a bolus composed primarily of small, firm balls of fine fur, loose coarse hair and bone. The bolus was sufficiently compact that it retained its shape after removal from the gizzard, and, although it was damp, moisture could not be squeezed from it. Only fragments of tissue from the larger muscle masses of the limbs remained; the tail was intact although little soft within
tissue could be detected visually. In the second sacrifice experiment, an owl was fed a total of three mice (a black one, then white, then black) at 2.5 hr intervals and sacrificed 0.5 hr after the last mouse was eaten. The first mouse ingested was completely digested within this 5.5 hr period. Digestion of the second mouse, ingested 3 hr before sacrifice, had not proceeded nearly as far in 3 hr as had digestion of the mouse fed as a “single-mouse meal” to the first owl sacrificed. The hind limbs were still attached to the pelvic girdle, muscle tissue remained on the bones, and neural tissue remained in the skull. The third mouse, at only 0.5 hr after ingestion, was intact and was resting at the cranial end of a rather wet bolus of gastric digestia from which fluid could be squeezed. In the third sacrifice experiment, a moist nearly formed pellet was found in the gizzard of an owl sacrificed 5 hr after having eaten 1.5 mice. Using a fourth owl, three mice were fed in two portions 5.0 hr apart and the owl was sacrificed 3 hr after the second por-
Time of day Fig. I. Frequencies of gastric contractions (detected by gastric extraluminal strain-gauge transducers) in a barred owl plotted by IOmin periods from food (mice) ingestion to pellet egestion for a meal eaten in one portion (A) or in three portions at I hr intervals (B). Interruptions in the plot indicate a failure to record data for a brief period usually due to technical difficulties.
t~on was eaten. The second portion was only partly digested after undergoing 3.0 hr of gastric digestion. Its appearance was similar to that of the second mouse ingested by the second sacrificed owl (above). When a fifth owl was sacrificed 12.0 hr after eating I.5 mice. a damp well-formed pellet of fur and bones was found in its gizzard. The last owl was fed 1.5 mice at 1900 hr. I.5 mice at 0700 hr. and sacrificed at 1000 hr. The I.5 mice making up the second portion of this meal were still almost completely articulated and were only minimally digested. The well digested remains of the first I.5 mouse-portion of the meal were interspersed with the second portion.
We found, as Chitty (3938) and Smith & Richmond (1972) had suggested. that the length of time required to digest food and egest a pellet increases when the daily food intake of an owl consists of several portions ingested over a period of time rather than all at once. Data obtained from our experiments more accurately reflect the ingestion schedule of wild owls and therefore their MPIs. The analyses of ingesta and recordings of gastric motility at various intervals after multiple feedings provide a more complete understanding of the influence of multiple daily feedings on the regulation of digestion. Patterns of gastric motility obtained via the extraluminal SGT in a barred owl were like those described previously for owls fed under similar conditions (Kostuch & Duke, 1975; Rhoades & Duke. 1978). As the barred owl swallowed food gastric motility increased during the “Filling Phase” (Phase 1). then decreased to a level maintained during “Early Chemical Digestion” (Phase II). and late ‘*Chemical Digestion” (Phase III) (Rhoades & Duke, 1978). The frequency of contractions gradually increased through “Early Pellet Compaction” (Phase IV) and “Late Pellet Compaction” (Phase V) until the maximum frequency of contractions was reached just prior to pellet egestion (Rhoades & Duke, 1978). When the barred owl was fed a second or third portion of its daily meal at 2.5 or 5 hr intervals, during Phase II, the motility reverted to Phase I within a few minutes. This renewed “Filling Phase” lasted about 0.25 I .SOhr, after which motility representative of chemical digestion resumed. Each time food was ingested after a previous portion had been partially digested. gastric motility was interrupted. it reverted to the filling stage. then resumed contraction patterns characteristic of chemical digestion. This delay in the digestive sequence was apparently partly responsible for the longer MPIs recorded from multiple feedings. While the motility pattern remained relatively constant through chemical digestion if not interrupted, the appearance of the ingesta in the ventriculus changed dramatically. Those three instances in which the contents of the GI tract of an owl were examined before a second portion was ingested allowed us to ascertain the phase of digestion (Rhoades & Duke, 1978) which had been reached. Three hours after ingestion of one mouse “Late Chemical Digestion” (Phase III) (Rhoades & Duke, 1978) was underway. When the ingesta were analyzed 30 min after the third of three portions fed at 2.5 hr intervals had been in-
gested (Sacrifice Experiment 2) the first mouse was found to have been thoroughly digested. but rhe second mouse. which had been in the
Regulation
of pellet egestion
tion with a second portion and apparently even more efficiently than if it had ingested the entire meal at one time. As several investigators have pointed out, the smaller the quantity ingested by an owl, the shorter the MPI (see Kostuch & Duke, 1975; Duke & Rhoades, 1977). The range of meal sizes fed in experiment 4 (Table 2) which produced two pellets in one 24 hr period, suggests that additional factors also influence MPI because both small and large meals resulted in two pellets/day. The size of the meal fed the previous day and thus the level of hunger of the owl is probably an additional factor affecting rates of digestion. Since only two of the four owls cast two pellets under this schedule individual variability may also be involved. Additionally, we have observed that an owl allowed to see food near the end of its expected MPI may egest a pellet earlier than expected. Perhaps the two owls which egested two pellets per day “anticipated” the second portion thus hastening the onset of pellet egestion. Whatever the cause of instances resulting in more rapid digestion of the first portion of the meal, the effect was a reduced time for the total daily ration. Fuller (1978) found that the natural activity patterns of free-ranging great-horned owls and barred owls often exhibited two peaks of activity, one beginning just before sunset and ending before midnight and another beginning about 0300 hr and ending near sunrise. This biphasic activity pattern is not uncommon among nocturnal animals (Aschoff, 1966). If an owl begins hunting soon after the onset of evening activity it may capture and ingest part of its daily nutritional requirements. Depending on the size of the portion ingested the owl may or may not egest a pellet before ingesting prey on the next morning. Egestion of a pellet from the evening meal would allow ingestion of a larger meal the next morning. The meal could be larger both relative to what might have been eaten if a pellet were not egested before eating and also relative to what was eaten on the previous evening. Eating a larger meal at sunrise than at dusk might be preferable since MPI for meals eaten at dawn was found to be shorter than for meals eaten in late afternoon (Duke & Rhoades, 1977) so a large meal at dawn might still be digested rapidly enough to permit pellet egestion before the evening hunt. Data of this nature provide a better understanding of factors affecting the regulation of digestion and they are valuable for strengthening models t!lat attempt to predict the most efficient predatory and bioenergetic strategies (e.g. Schoener, 1971). The data may also be applied to studies of owl food habits in which knowledge of the production of more than one pellet per day and MPI are essential for proper interpretation and quantification of food habits data (Howard, 1958; Marti, 1973).
443
Acknowledgements-We wish to thank J. E. Miller and P. S. Foxworthy for assistance during this study, and acknowledge support from NSF Grant GB 37254.
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