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Meal to pellet intervals in 14 species of captive raptors
Comp. BIochem Physial. 1976, VoL 53A, pp. I to 6 Pergamon Press. Printed in Great Britain
MEAL TO PELLET INTERVALS IN 14 SPECIES OF CAPTIVE RAPTORS* O. E. DUKE, O. A. EVANSON AND A. JEGERS Department of Veterinary Biology, College of Veterinary Medicine, Universlty of Minnesota, St. Paul, MN 55101, U.S.A.
(Received 15 January 1975) Abstract--1. In owls, meal to pellet interval was directly related to meal weight and owls normally cast 1 pellet per meal; egestlon of pellets in hawks apparently was associated with "lights-on" in the holding rooms regardless of quantity eaten and hawks normally egested less than 1 pellet per meal. 2. All of the smallest raptors digested meals and egested pellets more raptdly than the larger raptors. 3. The correlation between meal weight and pellet weight was only slightly better for owls than for hawks, but, because owl pellets contained more of the bones of their prey, they represented a greater proportion of the meal from which they originated. so that they had achieved a stable body weight prior to their use in experiments. The experiments were performed between January and June. Any physiological changes due to annual cycles occurring during this period were not believed to have significantly affected the parameters studled herein. The standard diet for experiments was laboratory mice (Mus musculus) and all birds were fed as much as they wanted during a 1 hour daily feeding period. The weights of the mice offered, of the uneaten food and of the raptors were determined (Toledo Scale, model 1070, Toledo, Ohio) and recorded. Body weights of the raptors were always determined after pellet egestion and before feeding. The weights of uneaten food items were corrected for dessication. No water for bathing or drinking was provided during experimental periods. The egestion of pellets was monitored in two ways. One method simply involved checking for pellets every 15 rain beginning prior to the tune that pellets were expected from each species. Visual checks could be made through a small hole in the door of each room without disturbing the birds. This system was used with the smaller owls (all but snowy and great-horned) whose egestion times were within the light period in the animal rooms. The method was also used wroth all of the hawks, except red-tails and goshawks, after it was learned that hawks usually egested pellets shortly after the lights came on in the animal rooms (see beyond). The egestion time for the few pellets which occurred m the dark, could be estimated by the degree of dessieation (i.e. weight loss) of the pellets when they were eventually collected. Also, pellets were observed to be "shiny" with moist mucus for about 30 rain after egestion; this condition was noted if observed at the time that the lights came on. The second method of monitoring egestion involved the use of automatic timing devices. With these devices egested pellets were directed, via a sloping chute under each bird, to a small wire mesh basket. The addition of a small (0"5g) weight (e.g. pellet) to this basket dosed a micrnswitch activating a circmt which caused a pen to mark a paper on a drum which rotated at a constant, known speed. Excreta reaching the basket passed through and did not close the microswitch. Since only four timing devices were available,, both monitoring methods were used simultaneously so that 8-10 birds could be tested at one time. All owls were fed at approximately 0900 and initial experiments with falconiforms also employed this feedlrlg time. Preliminary analysis of data revealed; however, that
INTRODUCTION PELLETS of undigestible food items are egested by many species of birds (Rea, 1973). Pellets have been used often in studies of food habits of raptors (e.g. Craighead & Craighead, 1969; Marti, 1969). The mechanisms of pellet formation and egestion and the meal to pellet interval (MPI), have not been as well studied. Recently, Balgooyen (1971) presented a brief listing of M P I data from apparently all previous investigations, and, only two other reports (Smith & Richmond, 1972; Duke et al., 1975) have since become available. The objectives of the present study were to determine M P I for as many species of raptors as possible and to gain insight into the regulation of pellet egestion and gastric digestion in raptors. MATERIALS AND METHODS Individuals from 14 species of raptors were used: 2 king vultures (Sarcorhamphus papa), 3 bald eagles (Hahaeetus leucocephalus), 4 northern goshawks (Acctp~ter gentilis), 2 broad-winged hawks (Buteo platypterus), 6 red-tailed hawks (Buteo jamaicensis), 3 rough-legged hawks (Buteo lagopus), 1 common caracara (Polyborus plancus), l American kestrel (Falco sparverms), 2 eastern screech owls (Otas asio), 4
great-horned owls (Bubo vtrgimanus), 2 snowy owls (Nyctea scandmca), 2 barred owls (Strix varia), 1 short-eared owl (Aszo flammeus), and 1 saw-whet owl (Aegolius acadtcus). The king vultures and caracara were on loan to us for 3 weeks from a local zoo. All the other species were available for this study from our raptor rehabihtatlon program. Durmg experiments all birds were housed in environmentally controlled rooms in which the temperature was maintained between 21-23°C, the relative humidity was kept between 40 to 50°//o,and the photoperiod was automatically timed to provide 14 hr of light between 0700 and 2100. The birds were jessed and kept on perches using standard falconry techniques. They were acclimated to the housing conditions and to the standard diet for 7-10 days before they were used m experiments. All birds were in good health and had been fed ad libitum for several weeks * This study was partially supported by National Science Foundation Grant No. NSF-GB 37254. C.B.P. S3/I A--A
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food consumed. A small sample size may have been responsible for the lack of a significant correlation between meal size and MPI in the saw-whet owl (Tables 2 and 3). This correlation was weaker in hawks. MPI in hawks appeared to be very greatly rclated to photopcriod; specifically, casting in hawks seemed to be associated with dawn (i.e. "lights-on" in our aniraal rooms). PcUct casting times for 2 red-tailed hawks and 2 goshawks were monitored automatically under conditions in which lights came on at 0700, TO PI~,J,0T Xk'L'EIVAL (IG~Z) AS UT..ATOD~Q ~ .
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As indicated above, most of the falconiforms were fed according to the latter schedule. However, individuals of two species, rough-legged hawks and kestrels, were not
available after the initial phases of the study for retesting on the 1I00 feeding schedule. The procedures used for determining dry matter consumption, dry weight of pellets,proportion of bones in pelletsand frequency of pelletregurgitationhave been previously described (Duke et al., 1975). In determining the proportion of each meal egested in a pellet and the coefficient of correlationbetween meal weight and pelletweight and between meal weight and MPI, a meal was defined as all food eaten since the last pellet.So, when a bird did not egest a pelleton some days but was fed everyday (e.g. all falconiforms), some of its "meals" and some of its pelletsactuallyrepresented 2 or 3 daily feedings. In computing MPI, the intervalsince the previous meal was used rather than the intervalsince the previous pellet. Mean values far MPI, daily dry matter consumption and body weight were used to calculate the MPI/g per kg and MPI/g.. For simplicity we will refer to all falconiforms used herein as hawks and to all strigiforms as owls.
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RESULTS
A very significant difference in M P I was found between hawks and owls. The average interval from feeding to egestion of a pellet in the various species of owls ranged from approximately 10-13 hr. In the hawk species, this interval averaged from 19-5-23-5 hr c . MPI in all of the owls except the sawwhet was strongly correlated with the quantity of
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Meal to lmllet intervals in captive raptors Tsblo 4~ h l l s t mst~nE times, u d e m s n ~ o d b y sm - ~ ' ~ _ ? b l n d w lind | o ~ b s w ] m . *
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the birds were fed at 1100 and they were not disturbed prior to 1100. In this test, approximately 77~ of the pellets of red-tails and 60% of the pellets of goshawks were cast between 0630 and 0830 (Table 4). Apparently dawn was sensed by these 4 hawks not only by photoperiodic clues. On weekends, when there was less traffic and noise within and outside of the building in which the birds were kept, casting times were slightly later (Table 4). If pellet casting in hawks occurred in preparation for eating, then birds fed at a regular time each day ought to cast at an approximately constant time interval prior to an anticipated feeding. When hawks were fed at 1100, MPI was always shorter than when the same birds were fed at 0900 (Table 1) thereby indicating that casting by the hawks in this study was more associated with the occurrence of dawn than with a preparation for, or anticipation of, being fed. Since average daily food intake for individuals of each species fed at 0900 was approximately equal or less (redTAISLS 5 :
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tailed hawks) than intake for individuals fed at 1100 (Table 5) yet, MPI was shorter in those individuals fed at ll00, meal size is again not indicated a s a factor determining MPI in hawks. Another major difference in pellet egestion between hawks and owls was the frequency of pellet egestion. All of the hawks commonly egested fewer than one pellet per meal on the average (Table 6). Some individual hawks cast more regularly than others, but, with the exception of the broad-winged hawks, hawks cast a pellet for only about 80°//0 of their meals. Broadwings egested one pellet for approximately every two meals. Our records indicated that during periods when birds were not casting, their daily food consumption declined until they eventually did cast. In contrast to hawks, it appeared to be normal for owls to cast a pellet for each meal (Table 6). The screech owls egested two pellets 1.5-2 hr apart on two occasions so their pellet casting frequency was slightly higher than one pellet per meal. Perhaps these were portions of the same pellet. The female snowy owl did not cast on one day but ate normally the next day. Neither of these situations is believed to be significant, but they have affected the pellet casting frequency data of the owls. Based on the MPI/g/kg (Table 3) it appears that smaller raptors digested meals and egested pellet relatively faster than larger ones. Also, food consumption per unit body weight was relatively greater for smaller birds as was expected. The goshawks and the shorteared owl were, however, exceptions (Table 5). These two species ate relatively more than expected for birds of their weight. Their MPI/g and MPI/g per kg were also rather low for birds of their size (Table 3) indicating a relatively more rapid digestion and pellet and egestion. The average proportion of a meal appearing as a pellet for goshawks and the short-eared owl was similar to that for the other hawks and owls, respectively (Table 6). Therefore, although they digested meals relatively more rapidly, they digested them approximately as well as other raptors. Owl pellets represented a larger proportion of the meal from which they originated than did those of hawks (Table 6). This difference is primarily due to TIBLJ 6.
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O. 'E: D u ~ ' O . A. EVANSONA N D A. JEOERS the prestmce ~f'much more osseous material in owl l~ollets than in the pellets of hawks (Table 6). However, the cort~elation between meal weight and pellet wright was only slightly better for owls than for hawks (Tabl~ 2), so, this correlation was little affected by the bone content of pellets. Therefore, regression lines (Fig. 1) were constructed for meal weight vs pellet weight for those species for which a significant correlation existed, between these two parameters. The'pellets oftbe smaller owls had a greater proportion of bones than did those of the larger owls (Table 6). This is probably due to the eating habit of the owls. The larger owls crushed the skulls of the mice and, the great-honed owls in particular usually crushed other bodes as well. The crushed bones would have been less likely to have survived gastric digestion and reappear in pellets. Although 2 king vultures were studied for 20 days, little aeeurate data were obtained because the birds "vomited" so frequently. This was a common "welcome" upon our entry into their holding room regardless of how discreetly we entered. Few well-formed pellets were cast. It was impossible to separate pellet material and partially digested food from the vomited mass and thus impossible to gather information on food requirements and pellet production on most days. Based on the limited data we did accumulate (Tables 5 and 6) and from notes on our observations, bone digestion, pellet formation and MPI in these vultures were apparently similar to these phenomena in other Falconiformes. Pellet egestion by vultures has been previously reported (Rea, 1973). The "vomiting" of the vultures was not observed in other raptors and to our knowledge'it has not been reported in other raptors. DISCUSSION
Probably the most significant results of the present study were those which demonstrated that hawks and owls were caused to egest pellets by two different stimuli. There is some indication from the scientific literature that this might be the case but it has not
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Fig. 1. Regression lines for meal weight vs the weight of the pellet from that meal. Regression lines were not ineluded for those species in which meal weight was not significantly correlated with pellet weight (Table 2). R.T. = red-tailed hawks, R.L. - rough-legged hawks, Gos. -- goshawl~s, Kest. = American Kestrel, Cara. -- Caraeara, S n . - Snowy owls, G.H.O.--great-horned owls, B.O. = barred owl, S.E.O. = short-eared owl, Ser. O. = Screech owl.
been previously postulated. Balgooyen (1971) fed three different diets (mice, small birds, and beef hearts plus cotton) to 4 American kestrels at 0900 daily. The birds were exposed to artifical light from 0800-1800. He found the mean MPI to be approximately 21.5 hr regardless of the nature of the diet or of the weight or volume consumed. He concluded that, "light regime and/or feeding time are the suspected determinants of when a pellet will be cast". Chitty (1938) studying a short-eared owl and Smith & Richmond (1972) in a study with a barn owl, found a direct correlation between the quantity consumed in a meal and the MPI for that meal. They also found that MPI's for given sized meals were longer at night than during the day, and that the MPI for one meal was shorter if a second meal was made available before egestion of the pellet from the first meal. Bond (1936) making field observations of falcons
(Falco peregrinus, Falco mexicanus, Falco sparverius, and Falco columbarius) indicated that casting occurred every morning, "ordinarily shortly after dawn". He also found that the two smaller species "may regurgitate a second pellet in the middle of the afternoon if the mornings' meal was eaten sufficiently early". Errington (1930) found that a captive juvenile marsh hawk regularly cast before 0800 each morning. However, if the bird was "fasted subsequent to a meal, he would disgorge a pellet of any size as soon as he had extracted the nourishment". These data agree with the theory that pellet egestion in hawks is associated with dawn. The data for the smaller species observed by Bond (1936) and for the fasted marsh hawk used by Errington (1933) do not agree with the data presented herein, but were collected under different experimental conditions. M P r s of owls have most frequently been studied in the great-horned owl and a wide range of values has been reported. Several authors have reported MPI's for this species to be in excess of 24 hr (Banks, 1884; Reed, 1925; Errington, 1938; Howard, 1958). Other reports have indicated that MPI for greath o n e d owls varies from 12 to 24 hr fReed & Reed, 1928; Errmgton, 1930; Grimm & Wh]tehouse, 1963; Duke et al., 1975). The data of the latter studies are more in agreement with the results of the present study. Sensing (1945) found that a barred owl eating mice always cast in less than 8 hr after eating. MPI for a short-eared owl fed small rodents during daylight hours varied from 1.5--13 hr but averaged about 8.5 hr for 30--40 g meals (Chitty, 1938). These intervals were shorter than those found herein for the same species. MPI's of 6.5-12 hr were reported for barn owls in four investigations (Guerin, 1928; Ticehurst, 1935; Wallace, 1948; Smith & Richmond, 1972). MPI data for a single species of owl probably vary due to the experimental conditions employed since as indicated above, factors in addition to meal size may have a minor influence on MPI in owls (Chitty, 1938; Smith & Richmond, 1972). In studies from tl~s laboratory, great-horned owls fed in the afternoon and thus casting at night (Duke et al., 1975) had longer MPI's than those in the present study which were fed at 0900. Also, the type of prey fed and the nutritional status of experimental birds may have influenced MPI's determined by previous investigators. While most of the available information on MPI's
Meal to pellet intervalrin captive raptors in owls does not indicate the mechanism(s), controlling the timing of casting, it does tend to indicate that pellet egestion in owls iLnot particularly associated with dawn. The failure of hawks to egest a pellet after each meal, as found in the present study, has been previously reported for red-tailed hawks, (Errington, 1930; Duke et al., 1975) red shoulcl~red hawks (Bueteo lineatus) (Errington, 1930), a golden eagle (Aquila chrysaetos) (Sumner, 1933), American kestrels (Bal-" gooyen, 1971), and 1 bald eagle (Duke et al., 1975). Redhead (1968) reported that portions of one meal may be distributed through several subsequent pellets in harrier hawks (Circus approximans gouldO. And, Balgooyen (1971) and Duke et al. (1975) have reported the occasional occurrence of more than one pellet from a single meal in American kest/els and in a gyrfalcon (Falco rusticolus), respectively. Most reports dealing with pellet egestion in owls have indicated that owls normally cast one pellet after each meal. There are, however, exceptions. Chitty (1938) found that one pellet from a short-eared owl may represent the indigestible portions-of two meals under certain conditions. Howard (1958) found that a great-horned owl did not cast every day and Marti (1973) found that a great-homed owl, long-eared owl (Asio otus), burrowing owl (Speotyto cunicularia), and a barn owl frequently cast more than one pellet per day. In the latter two studies food was available for long periods each day so that the number of meals taken per day by the birds was not certain. An explanation as to why hawks do not normally egest a pellet after each meal, while owls normally do, is not readily apparent. If food were scarce it might be beneficial for a bird to hold pellets longer in order to obtain all possible nutritional benefit from their food. But, an excess of food was available in the present study. Since hawks digest the bones of their prey more thoroughly than do owls, a smaller amount of each meal would be retained at the time of ingestion of a new meal by hawks. The presence of a pellet in the stomach of a hawk not only does not prevent it from eating, but also apparently does not act as the primary stimulus for pellet egestion. An external stimulus, viz. dawn, appears to be the primary stimulus or timer for hawks. In contrast, the presence of a pellet in the stomach of an owl appears to normally prevent it from eating. And, the size of the pellet, which is directly correlated with the size of the previous meal (which is directly correlated with MPI), appears to be the primary stimulus for pellet egestion, i.e. an internal stimulus. The chemical and/or physical nature of the pellet, or of the gastric environment at the end of the digestion of a meal when the pellet is formed, is probably also important in the stimulation of egestion in owls. The presence of a pellet in the stomach of hawks is apparently of less consequence than is the presence of a pellet in an owl's stomach. The short-eared owl and the goshawks ate relatively more than the other raptors in this study. The short-eared owl is more diurnal and is normally more active in hunting than the other species of owls used in this study (Mikkola, 1973). This greater activity may be associated with a higher inherent metabolic
5
rate. Our own observations of captive goshawks, and the observations of falconers (Beebe & Webster, 1964) indicate that ~ptive goshawks were mor~ .nervous and 'Tlighty" than the other hawks used in this study which probably accounts for their relatively higher food consumption. The presence of a much larger proportion of the bones of prey in owl pellets than in hawk pellets l ~ been previously reported by many autkors (e.g..Errington, 1930, 1932, 1933; Summer, 1933; Glading et al., 1943; Craighead & Craighead, 1969; Clark, 1972). More thorough bone digestion by hawks, due to greater acidity of the gastric juice of hawks as compared to owls (Duke et al., 1975), apparently explains the paucity of bones in hawk pellets. Several researchers have indicated that, because hawks digest bones so thoroughly, analysis of bones in hawk pellets is not a reliable way of determining the type and number of prey eaten (e.g. Errington, 1933; Redhead, 1968; Craighead & Craighead, 1969). It has recently been very clearly demonstrated (Raczynski & Ruprecht, 1974) that owl pellets are also not entirely,reliable sources of quantitative information on prey consumption. Regression lines for pellet weight vs food consumption such as those presented herein (Fig. 1), may be useful in estimating the mass eaten to produce a pellet of a given, known dry weight. The present data apply only to a diet of mice, however, similar data could be obtained for other diets. The results of this study were obtained under standard, but unnatural conditions. For example, all of the daily food requirements for each bird were provided at one daily feeding. Probably most raptors require several hours, if not most of the day or night, to catch their daily requirement of small rodents. It would be interesting to determine MPI for raptor species in experiments in which mice are fed one at a time for 2-3 hr, or two meals are fed each day. It would also be interesting to see if "hungry" hawks (as opposed to our well-fed specimens) would cast with greater or less frequency and if hungry owls might cast after a longer MPI. SUMMARY
Meal to pellet intervals (MPI~ food consumption, pellet production and the interrelationships of these phenomena were studied in six species of owls and eight falconiform species. MPI was directly correlated with meal weight in owls and averaged 10-13 hr for the species tested. MPI and meal weight were not as well correlated, in hawks. Pellet egestion averaged 19.5-23-5 hr in the various species of hawks and appeared to be associated with dawn. Owls normally egested one pellet after each meal whereas, hawks often ate two or three meals before casting a pellet. The MPI/g eaten per kg of body weight was shortest for goshawks, a short-eared owl and all of the smallest raptors. Owl pellets represented a larger proportion of the meal from which they originated than did hawk pellets because owl pellets contained 10-12 times more bone material than those of hawks.
Acknowledoement.~We are vary grateful to Mr. John Fletcher of the Como l~ark Zoo, St. Patti',- Mifinesota, for
6
G . E . DUK~ O. A. EVANSON A N D A. JEGERS
the use of 2 king vultures and a caracara in this study. The technical assistance of Mr. Randall L. Herman, Mr. Thomas Kleinart, Mr. Thomas E. Kostuch, Ms. Victoria Kramer and Mr. Roger P. Pitts was greatly appreciated.
REFERENCES BALC,OOV~q T. G. (1971) Pellet regurgitaUon by captive sparrow hawks (Falco sparverius). Condor 73, 382-385 BANKSJ. W. (1884) The great horned owl in confinement. Auk 1, 194-195. BEEaE F. L. & WEBSTERH. M. (1964) North American Falconry and Hunting Hawks, p. 315. World Press, Denver, Colorado. BOND R. M. 0936) Eating habits of falcons with special reference to pellet analysis. Condor 38, 72-76 CtlrrrY D. (1938) Pellet formation in short-eared owls, Asio flammeus. Proc zool Soc J..ond. 108 (Ser. A), 267-287. CLARK R. J. (1972) Pellets of the short-eared owl and marsh hawks compared. J. Frffdl. M.qt. 36, 962-964. CRAIGHEAD J. J. & CRAIGHEADF. C, JR. 0969) Hawks, Owls and Wildlife, p 443, Second Ed Dover Pub. New York. DUKE G. E.,,JEO~s A. A., LOFF G. & EV^NSON O. A. (1975) Gastric dlgesnon m some raptors. Comp. Biochem. Physiol. 50A, 649-656. ERRIN(3TOSP. L. (1930) The pellet analysis method of raptor food habits study. Condor 32, 292-296. ERP,tNGTON P. L. 0932) Techmque of raptor food habits study. Condor 34, 75-86. ERRn~GTON P. L. (1933) Food habits of Southern Wisconsin raptors. Part II-Hawks. Condor 35, 19-29. ERRn~GTON P. L. (1938) The great-horned owl as an indicator of vulnerability m prey populations. J. [,HIdl. Mot. 2, 190-205. GLADING B., TILLOTSON D. F. & SELLECK D. M. (1943) Raptor pellets as indicators of food habits. Calif. Fish Game 29, 92-121.
GRIMM R J. & Whitehouse W. M. 0963) Pellet formation in a great-horned owl: a roentgenographic study. Auk 80, 301-306. Gu~n~ G. (1928) La vie des chouettes. Regime et crolssance de reffraye commune Tj~toalba alba (L.) en vend6e, p. 157. P. Lechevalier, Paris. In CHrrrv D. (1938) above. HOWARD W. E. (1958) Food intake and pellet formation of a horned owl V~lson Bull. 70, 145-150. MART1C D. (1969) Some comparisons of the feeding ecology of four owls in north central Colorado. SW Nat. 14, 163-170. MART1 C. D. (1973) Food consumption and pellet formation rates in four owl species. B~lson Bull. 85, 178-181. MIKKOLA H. (1973) Wood Owls. In Owls of the World (Edited by BURTON J. A.), p. 216. E. P. Dutton. New York. RACZYNSKIJ & RUPREerrr A. L. 0974) The effect of digestion on the osteologleal composition of owl pellets. Acta Ornith. 14, 25-38. REA A. M. (1973) Turkey vultures casting pellets. Auk 90, 209-210 REDHEADR. E. (1968) An analysis of pellets cast by harrier hawks. Notornis 15, 244-247. REED B. P. 0925) Growth, development and reactions of young great horned owls. Auk 42, 14--31. RE~D C I. & REED B. P. (1928) The mechanism of pellet formation in the great horned owl (Bubo varginianus). Science, N Y. 68, 359-360. SENSINGE. C (1945)The formation of pellets by the barred owl. H41son Bull. 57, 132. SMITh C. R. & RICHMONDM E. (1972) Factors influencing pellet egestion and gastric p H m the barn owl. H41son Bull. 84, 179-186. SUMNER E. L. (1933) The growth of some young raptorial birds. Univ. Cal. Pubis. Zool. 40, 277-308. TICF~URST C. B (1935) On the food of the barn owl and its bearing on barn owl population. Ibis 5, 329-335. WALLACE G. J. (1948) The barn owl in Michigan. Tech. Bull. Mich. (St. Coil) Agrzc. Exp. Sta. 280, 1-61.
MEAL TO PELLET INTERVALS IN 14 SPECIES OF CAPTIVE RAPTORS* O. E. DUKE, O. A. EVANSON AND A. JEGERS Department of Veterinary Biology, College of Veterinary Medicine, Universlty of Minnesota, St. Paul, MN 55101, U.S.A.
(Received 15 January 1975) Abstract--1. In owls, meal to pellet interval was directly related to meal weight and owls normally cast 1 pellet per meal; egestlon of pellets in hawks apparently was associated with "lights-on" in the holding rooms regardless of quantity eaten and hawks normally egested less than 1 pellet per meal. 2. All of the smallest raptors digested meals and egested pellets more raptdly than the larger raptors. 3. The correlation between meal weight and pellet weight was only slightly better for owls than for hawks, but, because owl pellets contained more of the bones of their prey, they represented a greater proportion of the meal from which they originated. so that they had achieved a stable body weight prior to their use in experiments. The experiments were performed between January and June. Any physiological changes due to annual cycles occurring during this period were not believed to have significantly affected the parameters studled herein. The standard diet for experiments was laboratory mice (Mus musculus) and all birds were fed as much as they wanted during a 1 hour daily feeding period. The weights of the mice offered, of the uneaten food and of the raptors were determined (Toledo Scale, model 1070, Toledo, Ohio) and recorded. Body weights of the raptors were always determined after pellet egestion and before feeding. The weights of uneaten food items were corrected for dessication. No water for bathing or drinking was provided during experimental periods. The egestion of pellets was monitored in two ways. One method simply involved checking for pellets every 15 rain beginning prior to the tune that pellets were expected from each species. Visual checks could be made through a small hole in the door of each room without disturbing the birds. This system was used with the smaller owls (all but snowy and great-horned) whose egestion times were within the light period in the animal rooms. The method was also used wroth all of the hawks, except red-tails and goshawks, after it was learned that hawks usually egested pellets shortly after the lights came on in the animal rooms (see beyond). The egestion time for the few pellets which occurred m the dark, could be estimated by the degree of dessieation (i.e. weight loss) of the pellets when they were eventually collected. Also, pellets were observed to be "shiny" with moist mucus for about 30 rain after egestion; this condition was noted if observed at the time that the lights came on. The second method of monitoring egestion involved the use of automatic timing devices. With these devices egested pellets were directed, via a sloping chute under each bird, to a small wire mesh basket. The addition of a small (0"5g) weight (e.g. pellet) to this basket dosed a micrnswitch activating a circmt which caused a pen to mark a paper on a drum which rotated at a constant, known speed. Excreta reaching the basket passed through and did not close the microswitch. Since only four timing devices were available,, both monitoring methods were used simultaneously so that 8-10 birds could be tested at one time. All owls were fed at approximately 0900 and initial experiments with falconiforms also employed this feedlrlg time. Preliminary analysis of data revealed; however, that
INTRODUCTION PELLETS of undigestible food items are egested by many species of birds (Rea, 1973). Pellets have been used often in studies of food habits of raptors (e.g. Craighead & Craighead, 1969; Marti, 1969). The mechanisms of pellet formation and egestion and the meal to pellet interval (MPI), have not been as well studied. Recently, Balgooyen (1971) presented a brief listing of M P I data from apparently all previous investigations, and, only two other reports (Smith & Richmond, 1972; Duke et al., 1975) have since become available. The objectives of the present study were to determine M P I for as many species of raptors as possible and to gain insight into the regulation of pellet egestion and gastric digestion in raptors. MATERIALS AND METHODS Individuals from 14 species of raptors were used: 2 king vultures (Sarcorhamphus papa), 3 bald eagles (Hahaeetus leucocephalus), 4 northern goshawks (Acctp~ter gentilis), 2 broad-winged hawks (Buteo platypterus), 6 red-tailed hawks (Buteo jamaicensis), 3 rough-legged hawks (Buteo lagopus), 1 common caracara (Polyborus plancus), l American kestrel (Falco sparverms), 2 eastern screech owls (Otas asio), 4
great-horned owls (Bubo vtrgimanus), 2 snowy owls (Nyctea scandmca), 2 barred owls (Strix varia), 1 short-eared owl (Aszo flammeus), and 1 saw-whet owl (Aegolius acadtcus). The king vultures and caracara were on loan to us for 3 weeks from a local zoo. All the other species were available for this study from our raptor rehabihtatlon program. Durmg experiments all birds were housed in environmentally controlled rooms in which the temperature was maintained between 21-23°C, the relative humidity was kept between 40 to 50°//o,and the photoperiod was automatically timed to provide 14 hr of light between 0700 and 2100. The birds were jessed and kept on perches using standard falconry techniques. They were acclimated to the housing conditions and to the standard diet for 7-10 days before they were used m experiments. All birds were in good health and had been fed ad libitum for several weeks * This study was partially supported by National Science Foundation Grant No. NSF-GB 37254. C.B.P. S3/I A--A
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A very significant difference in M P I was found between hawks and owls. The average interval from feeding to egestion of a pellet in the various species of owls ranged from approximately 10-13 hr. In the hawk species, this interval averaged from 19-5-23-5 hr c . MPI in all of the owls except the sawwhet was strongly correlated with the quantity of
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the birds were fed at 1100 and they were not disturbed prior to 1100. In this test, approximately 77~ of the pellets of red-tails and 60% of the pellets of goshawks were cast between 0630 and 0830 (Table 4). Apparently dawn was sensed by these 4 hawks not only by photoperiodic clues. On weekends, when there was less traffic and noise within and outside of the building in which the birds were kept, casting times were slightly later (Table 4). If pellet casting in hawks occurred in preparation for eating, then birds fed at a regular time each day ought to cast at an approximately constant time interval prior to an anticipated feeding. When hawks were fed at 1100, MPI was always shorter than when the same birds were fed at 0900 (Table 1) thereby indicating that casting by the hawks in this study was more associated with the occurrence of dawn than with a preparation for, or anticipation of, being fed. Since average daily food intake for individuals of each species fed at 0900 was approximately equal or less (redTAISLS 5 :
I ~ J I BODY vlrr.~HTS AN~ i~ff,S.q DXT 14A.11"~ (D .H. ) C ~ r S 0 H ~ FOR 16 S~BCZES OF I A P T Q U .
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tailed hawks) than intake for individuals fed at 1100 (Table 5) yet, MPI was shorter in those individuals fed at ll00, meal size is again not indicated a s a factor determining MPI in hawks. Another major difference in pellet egestion between hawks and owls was the frequency of pellet egestion. All of the hawks commonly egested fewer than one pellet per meal on the average (Table 6). Some individual hawks cast more regularly than others, but, with the exception of the broad-winged hawks, hawks cast a pellet for only about 80°//0 of their meals. Broadwings egested one pellet for approximately every two meals. Our records indicated that during periods when birds were not casting, their daily food consumption declined until they eventually did cast. In contrast to hawks, it appeared to be normal for owls to cast a pellet for each meal (Table 6). The screech owls egested two pellets 1.5-2 hr apart on two occasions so their pellet casting frequency was slightly higher than one pellet per meal. Perhaps these were portions of the same pellet. The female snowy owl did not cast on one day but ate normally the next day. Neither of these situations is believed to be significant, but they have affected the pellet casting frequency data of the owls. Based on the MPI/g/kg (Table 3) it appears that smaller raptors digested meals and egested pellet relatively faster than larger ones. Also, food consumption per unit body weight was relatively greater for smaller birds as was expected. The goshawks and the shorteared owl were, however, exceptions (Table 5). These two species ate relatively more than expected for birds of their weight. Their MPI/g and MPI/g per kg were also rather low for birds of their size (Table 3) indicating a relatively more rapid digestion and pellet and egestion. The average proportion of a meal appearing as a pellet for goshawks and the short-eared owl was similar to that for the other hawks and owls, respectively (Table 6). Therefore, although they digested meals relatively more rapidly, they digested them approximately as well as other raptors. Owl pellets represented a larger proportion of the meal from which they originated than did those of hawks (Table 6). This difference is primarily due to TIBLJ 6.
0900 It
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•
O. 'E: D u ~ ' O . A. EVANSONA N D A. JEOERS the prestmce ~f'much more osseous material in owl l~ollets than in the pellets of hawks (Table 6). However, the cort~elation between meal weight and pellet wright was only slightly better for owls than for hawks (Tabl~ 2), so, this correlation was little affected by the bone content of pellets. Therefore, regression lines (Fig. 1) were constructed for meal weight vs pellet weight for those species for which a significant correlation existed, between these two parameters. The'pellets oftbe smaller owls had a greater proportion of bones than did those of the larger owls (Table 6). This is probably due to the eating habit of the owls. The larger owls crushed the skulls of the mice and, the great-honed owls in particular usually crushed other bodes as well. The crushed bones would have been less likely to have survived gastric digestion and reappear in pellets. Although 2 king vultures were studied for 20 days, little aeeurate data were obtained because the birds "vomited" so frequently. This was a common "welcome" upon our entry into their holding room regardless of how discreetly we entered. Few well-formed pellets were cast. It was impossible to separate pellet material and partially digested food from the vomited mass and thus impossible to gather information on food requirements and pellet production on most days. Based on the limited data we did accumulate (Tables 5 and 6) and from notes on our observations, bone digestion, pellet formation and MPI in these vultures were apparently similar to these phenomena in other Falconiformes. Pellet egestion by vultures has been previously reported (Rea, 1973). The "vomiting" of the vultures was not observed in other raptors and to our knowledge'it has not been reported in other raptors. DISCUSSION
Probably the most significant results of the present study were those which demonstrated that hawks and owls were caused to egest pellets by two different stimuli. There is some indication from the scientific literature that this might be the case but it has not
/-.
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l
Io
l
I
P
l
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20 30 40 50 6O 70 Consumption of mice, g dry m o i ' t e r l k g
I
80
I
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Fig. 1. Regression lines for meal weight vs the weight of the pellet from that meal. Regression lines were not ineluded for those species in which meal weight was not significantly correlated with pellet weight (Table 2). R.T. = red-tailed hawks, R.L. - rough-legged hawks, Gos. -- goshawl~s, Kest. = American Kestrel, Cara. -- Caraeara, S n . - Snowy owls, G.H.O.--great-horned owls, B.O. = barred owl, S.E.O. = short-eared owl, Ser. O. = Screech owl.
been previously postulated. Balgooyen (1971) fed three different diets (mice, small birds, and beef hearts plus cotton) to 4 American kestrels at 0900 daily. The birds were exposed to artifical light from 0800-1800. He found the mean MPI to be approximately 21.5 hr regardless of the nature of the diet or of the weight or volume consumed. He concluded that, "light regime and/or feeding time are the suspected determinants of when a pellet will be cast". Chitty (1938) studying a short-eared owl and Smith & Richmond (1972) in a study with a barn owl, found a direct correlation between the quantity consumed in a meal and the MPI for that meal. They also found that MPI's for given sized meals were longer at night than during the day, and that the MPI for one meal was shorter if a second meal was made available before egestion of the pellet from the first meal. Bond (1936) making field observations of falcons
(Falco peregrinus, Falco mexicanus, Falco sparverius, and Falco columbarius) indicated that casting occurred every morning, "ordinarily shortly after dawn". He also found that the two smaller species "may regurgitate a second pellet in the middle of the afternoon if the mornings' meal was eaten sufficiently early". Errington (1930) found that a captive juvenile marsh hawk regularly cast before 0800 each morning. However, if the bird was "fasted subsequent to a meal, he would disgorge a pellet of any size as soon as he had extracted the nourishment". These data agree with the theory that pellet egestion in hawks is associated with dawn. The data for the smaller species observed by Bond (1936) and for the fasted marsh hawk used by Errington (1933) do not agree with the data presented herein, but were collected under different experimental conditions. M P r s of owls have most frequently been studied in the great-horned owl and a wide range of values has been reported. Several authors have reported MPI's for this species to be in excess of 24 hr (Banks, 1884; Reed, 1925; Errington, 1938; Howard, 1958). Other reports have indicated that MPI for greath o n e d owls varies from 12 to 24 hr fReed & Reed, 1928; Errmgton, 1930; Grimm & Wh]tehouse, 1963; Duke et al., 1975). The data of the latter studies are more in agreement with the results of the present study. Sensing (1945) found that a barred owl eating mice always cast in less than 8 hr after eating. MPI for a short-eared owl fed small rodents during daylight hours varied from 1.5--13 hr but averaged about 8.5 hr for 30--40 g meals (Chitty, 1938). These intervals were shorter than those found herein for the same species. MPI's of 6.5-12 hr were reported for barn owls in four investigations (Guerin, 1928; Ticehurst, 1935; Wallace, 1948; Smith & Richmond, 1972). MPI data for a single species of owl probably vary due to the experimental conditions employed since as indicated above, factors in addition to meal size may have a minor influence on MPI in owls (Chitty, 1938; Smith & Richmond, 1972). In studies from tl~s laboratory, great-horned owls fed in the afternoon and thus casting at night (Duke et al., 1975) had longer MPI's than those in the present study which were fed at 0900. Also, the type of prey fed and the nutritional status of experimental birds may have influenced MPI's determined by previous investigators. While most of the available information on MPI's
Meal to pellet intervalrin captive raptors in owls does not indicate the mechanism(s), controlling the timing of casting, it does tend to indicate that pellet egestion in owls iLnot particularly associated with dawn. The failure of hawks to egest a pellet after each meal, as found in the present study, has been previously reported for red-tailed hawks, (Errington, 1930; Duke et al., 1975) red shoulcl~red hawks (Bueteo lineatus) (Errington, 1930), a golden eagle (Aquila chrysaetos) (Sumner, 1933), American kestrels (Bal-" gooyen, 1971), and 1 bald eagle (Duke et al., 1975). Redhead (1968) reported that portions of one meal may be distributed through several subsequent pellets in harrier hawks (Circus approximans gouldO. And, Balgooyen (1971) and Duke et al. (1975) have reported the occasional occurrence of more than one pellet from a single meal in American kest/els and in a gyrfalcon (Falco rusticolus), respectively. Most reports dealing with pellet egestion in owls have indicated that owls normally cast one pellet after each meal. There are, however, exceptions. Chitty (1938) found that one pellet from a short-eared owl may represent the indigestible portions-of two meals under certain conditions. Howard (1958) found that a great-horned owl did not cast every day and Marti (1973) found that a great-homed owl, long-eared owl (Asio otus), burrowing owl (Speotyto cunicularia), and a barn owl frequently cast more than one pellet per day. In the latter two studies food was available for long periods each day so that the number of meals taken per day by the birds was not certain. An explanation as to why hawks do not normally egest a pellet after each meal, while owls normally do, is not readily apparent. If food were scarce it might be beneficial for a bird to hold pellets longer in order to obtain all possible nutritional benefit from their food. But, an excess of food was available in the present study. Since hawks digest the bones of their prey more thoroughly than do owls, a smaller amount of each meal would be retained at the time of ingestion of a new meal by hawks. The presence of a pellet in the stomach of a hawk not only does not prevent it from eating, but also apparently does not act as the primary stimulus for pellet egestion. An external stimulus, viz. dawn, appears to be the primary stimulus or timer for hawks. In contrast, the presence of a pellet in the stomach of an owl appears to normally prevent it from eating. And, the size of the pellet, which is directly correlated with the size of the previous meal (which is directly correlated with MPI), appears to be the primary stimulus for pellet egestion, i.e. an internal stimulus. The chemical and/or physical nature of the pellet, or of the gastric environment at the end of the digestion of a meal when the pellet is formed, is probably also important in the stimulation of egestion in owls. The presence of a pellet in the stomach of hawks is apparently of less consequence than is the presence of a pellet in an owl's stomach. The short-eared owl and the goshawks ate relatively more than the other raptors in this study. The short-eared owl is more diurnal and is normally more active in hunting than the other species of owls used in this study (Mikkola, 1973). This greater activity may be associated with a higher inherent metabolic
5
rate. Our own observations of captive goshawks, and the observations of falconers (Beebe & Webster, 1964) indicate that ~ptive goshawks were mor~ .nervous and 'Tlighty" than the other hawks used in this study which probably accounts for their relatively higher food consumption. The presence of a much larger proportion of the bones of prey in owl pellets than in hawk pellets l ~ been previously reported by many autkors (e.g..Errington, 1930, 1932, 1933; Summer, 1933; Glading et al., 1943; Craighead & Craighead, 1969; Clark, 1972). More thorough bone digestion by hawks, due to greater acidity of the gastric juice of hawks as compared to owls (Duke et al., 1975), apparently explains the paucity of bones in hawk pellets. Several researchers have indicated that, because hawks digest bones so thoroughly, analysis of bones in hawk pellets is not a reliable way of determining the type and number of prey eaten (e.g. Errington, 1933; Redhead, 1968; Craighead & Craighead, 1969). It has recently been very clearly demonstrated (Raczynski & Ruprecht, 1974) that owl pellets are also not entirely,reliable sources of quantitative information on prey consumption. Regression lines for pellet weight vs food consumption such as those presented herein (Fig. 1), may be useful in estimating the mass eaten to produce a pellet of a given, known dry weight. The present data apply only to a diet of mice, however, similar data could be obtained for other diets. The results of this study were obtained under standard, but unnatural conditions. For example, all of the daily food requirements for each bird were provided at one daily feeding. Probably most raptors require several hours, if not most of the day or night, to catch their daily requirement of small rodents. It would be interesting to determine MPI for raptor species in experiments in which mice are fed one at a time for 2-3 hr, or two meals are fed each day. It would also be interesting to see if "hungry" hawks (as opposed to our well-fed specimens) would cast with greater or less frequency and if hungry owls might cast after a longer MPI. SUMMARY
Meal to pellet intervals (MPI~ food consumption, pellet production and the interrelationships of these phenomena were studied in six species of owls and eight falconiform species. MPI was directly correlated with meal weight in owls and averaged 10-13 hr for the species tested. MPI and meal weight were not as well correlated, in hawks. Pellet egestion averaged 19.5-23-5 hr in the various species of hawks and appeared to be associated with dawn. Owls normally egested one pellet after each meal whereas, hawks often ate two or three meals before casting a pellet. The MPI/g eaten per kg of body weight was shortest for goshawks, a short-eared owl and all of the smallest raptors. Owl pellets represented a larger proportion of the meal from which they originated than did hawk pellets because owl pellets contained 10-12 times more bone material than those of hawks.
Acknowledoement.~We are vary grateful to Mr. John Fletcher of the Como l~ark Zoo, St. Patti',- Mifinesota, for
6
G . E . DUK~ O. A. EVANSON A N D A. JEGERS
the use of 2 king vultures and a caracara in this study. The technical assistance of Mr. Randall L. Herman, Mr. Thomas Kleinart, Mr. Thomas E. Kostuch, Ms. Victoria Kramer and Mr. Roger P. Pitts was greatly appreciated.
REFERENCES BALC,OOV~q T. G. (1971) Pellet regurgitaUon by captive sparrow hawks (Falco sparverius). Condor 73, 382-385 BANKSJ. W. (1884) The great horned owl in confinement. Auk 1, 194-195. BEEaE F. L. & WEBSTERH. M. (1964) North American Falconry and Hunting Hawks, p. 315. World Press, Denver, Colorado. BOND R. M. 0936) Eating habits of falcons with special reference to pellet analysis. Condor 38, 72-76 CtlrrrY D. (1938) Pellet formation in short-eared owls, Asio flammeus. Proc zool Soc J..ond. 108 (Ser. A), 267-287. CLARK R. J. (1972) Pellets of the short-eared owl and marsh hawks compared. J. Frffdl. M.qt. 36, 962-964. CRAIGHEAD J. J. & CRAIGHEADF. C, JR. 0969) Hawks, Owls and Wildlife, p 443, Second Ed Dover Pub. New York. DUKE G. E.,,JEO~s A. A., LOFF G. & EV^NSON O. A. (1975) Gastric dlgesnon m some raptors. Comp. Biochem. Physiol. 50A, 649-656. ERRIN(3TOSP. L. (1930) The pellet analysis method of raptor food habits study. Condor 32, 292-296. ERP,tNGTON P. L. 0932) Techmque of raptor food habits study. Condor 34, 75-86. ERRn~GTON P. L. (1933) Food habits of Southern Wisconsin raptors. Part II-Hawks. Condor 35, 19-29. ERRn~GTON P. L. (1938) The great-horned owl as an indicator of vulnerability m prey populations. J. [,HIdl. Mot. 2, 190-205. GLADING B., TILLOTSON D. F. & SELLECK D. M. (1943) Raptor pellets as indicators of food habits. Calif. Fish Game 29, 92-121.
GRIMM R J. & Whitehouse W. M. 0963) Pellet formation in a great-horned owl: a roentgenographic study. Auk 80, 301-306. Gu~n~ G. (1928) La vie des chouettes. Regime et crolssance de reffraye commune Tj~toalba alba (L.) en vend6e, p. 157. P. Lechevalier, Paris. In CHrrrv D. (1938) above. HOWARD W. E. (1958) Food intake and pellet formation of a horned owl V~lson Bull. 70, 145-150. MART1C D. (1969) Some comparisons of the feeding ecology of four owls in north central Colorado. SW Nat. 14, 163-170. MART1 C. D. (1973) Food consumption and pellet formation rates in four owl species. B~lson Bull. 85, 178-181. MIKKOLA H. (1973) Wood Owls. In Owls of the World (Edited by BURTON J. A.), p. 216. E. P. Dutton. New York. RACZYNSKIJ & RUPREerrr A. L. 0974) The effect of digestion on the osteologleal composition of owl pellets. Acta Ornith. 14, 25-38. REA A. M. (1973) Turkey vultures casting pellets. Auk 90, 209-210 REDHEADR. E. (1968) An analysis of pellets cast by harrier hawks. Notornis 15, 244-247. REED B. P. 0925) Growth, development and reactions of young great horned owls. Auk 42, 14--31. RE~D C I. & REED B. P. (1928) The mechanism of pellet formation in the great horned owl (Bubo varginianus). Science, N Y. 68, 359-360. SENSINGE. C (1945)The formation of pellets by the barred owl. H41son Bull. 57, 132. SMITh C. R. & RICHMONDM E. (1972) Factors influencing pellet egestion and gastric p H m the barn owl. H41son Bull. 84, 179-186. SUMNER E. L. (1933) The growth of some young raptorial birds. Univ. Cal. Pubis. Zool. 40, 277-308. TICF~URST C. B (1935) On the food of the barn owl and its bearing on barn owl population. Ibis 5, 329-335. WALLACE G. J. (1948) The barn owl in Michigan. Tech. Bull. Mich. (St. Coil) Agrzc. Exp. Sta. 280, 1-61.