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j RaptorRes. 30(4):219-223 ¸ 1996 The Raptor ResearchFoundation, Inc.

FACTORS INFLUENCING THE SIZE OF SOME INTERNAL ORGANS IN RAPTORS

NIGEL W. BARTON AND DAVID C. HOUSTON AppliedOrnithology Unit, Divisionof Evolutionaryand EnvironmentalBiology, Graham Kerr Building, Universityof Glasgow,Glasgow, G12 8Q•

ABSTP•CT.--Thesize of the small intestine, stomach, kidney, liver and heart were compared among raptor speciesand considered in relation to hunting strategyand body size. Speciesrelying on rapid accelerationand maneuverabilityto captureprey in flight, suchas sparrowhawk (Accipiter nisus), goshawk (A. gentilis),and peregrine (Falcoperegrinus), had the smallestdigestive tracts for their size. Species depending more on soaringflight which do not need fast accelerationto capture prey,such as (Buteobuteo), red kite (Milvus milvus), and European kestrel (Falco tinnunculus),had heavy digestiveorgans. In the Strigiformes,the same relationship wasfound, and specieswhich hunt by active flight, such as barn (Tyt0 alba), and 1ong-earedowl (Asio otus),had significantlylighter digestive tracts than the tawny owl ( aluco),a specieswhich mainly hunts from a perch dropping onto its prey from above.Body condition waspositively correlated with organ weights,including the heart, but to a lesserextent with linear measuresof size such as intestine length. KEYWOe. DS: internalorgans; predatory ; condition.

Factoresque infiuencian el tamafio de algunos6rganos internos en rapaces RESUMEN.--EItamafio del intestinodelgado, est6mago, riffones, higado y coraz6n,rue comparadoentre especiesde rapacesque difieren en estrategiade caza y tamafio corporal. Especiesbasadas en r•pida aceleraci6ny maniobrabilidadpara capturarpresas en vuelo, talescomo Accipiternisus, A. gentilisy Falco peregrinusten/an el tracto digestivom•s pequefio para su tamafio corporal. Especiesque dependen m•s bien de un vuelo de planeo y que no necesitande una r•pida aceleraci6n,tales como Buteobuteo, Milvus milvusy Falcotinnunculus, tenlan 6rganosdigestivos m:is pesados.En Strigiformesse encontr6 la misma relaci6n, especiesque cazan por vuelo activo,tales como Tytoalba, Asio otus, ten/an un tracto digestivo significativamentem•s liviano que Atrix aluco,una especieque caza esperandoa la presa desde una percha. La condici6n corporal estuvocorrelacionada positivamente con el pesode los 6rganos,inclu- yendo el coraz6n. [Traducci6n de Ivan Lazo]

We previouslyreported that birds of prey show sociation between the length of the small intestine considerablevariation in the length of their small and the predatory strategyshown by a species,and intestines (Barton and Houston 1994) and sug- that after correcting for differences in body size, gestedthat these differences could be due to ad- those species that specialized in the capture of aptationsfor different stylesof . We hy- small birds in flight had small intestinallengths up pothesized that raptors which capture prey by to 50% shorter than specieswith a lessactive pred- pouncing on it from abovewould have the longest atory style. The small intestine is responsiblefor gut lengths for efficient digestion while species nutrient absorption and is therefore the organ which need to acceleraterapidly to capture active most likely to effect absorptionefficiency. We have prey, such as predators taking small prey in flight, shown that specieswith short small intestines di- would have very light organ systemsto enable gest their food less efficiently, and as a conse- them to acceleratemore rapidly. Reduction in the quence select only prey items of high energy con- length of the small intestine probably resultsin less tent (Barton and Houston 1993a, 1993b). efficient absorption of food but this could still be This paper considerswhether there may be as- selected for if this disadvantagewere more than sociations between predatory strategy and the compensatedfor by a higher rate of prey capture. weight of other organ systems.We compared the We were able to demonstrate that there was an as- massof the gizzard, proventriculus,small intestine,

219 220 N. BARTON AND D. HOUSTON VOL. 30, NO. 4

Table 1. Mean wet weights (_SD) of internal organs of various raptors expressedas a percentage of total body weight. Means are basedon a combination of the sizesof internal organsof both sexesand samplesizes are given in parentheses.

SMALL BODY SPECIES LWER HEART KIDNEY STOMACH INTESTINE M_ASS

Kestrel 3.24 -+ 0.46 (14) 1.13 -+ 0.14 (12) 1.14_+ 0.22 (10) 2.62 +- 0.34 (12) 0.75 _+0.42 (18) 180 Merlin 3.24 -+ 0.84 (3) 2.20 +- 0.31 (3) 1.1o (1) 1.56 ___0.32 (3) 0.56 (1) 190 Sparrowhawk 2.63 -+ 0.53 (86) 1.12 +_0.14 (75) 0.81 ___0.12 (59) 0.95 -+ 0.13 (38) 0.63 _+0.28 (22) 220 Peregrine 2.76 +_0.43 (3) 1.81 _+0.05 (3) 0.86_+0.2 (3) 1.24 (1) 0.53 +_0.05 (3) 760 Buzzard 2.15 +_0.47 (5) 0.86 +_0.15 (31) 0.92 +_0.05 (3) 1.48 _+0.41 (4) 0.99 _+2.62 (7) 850 Red Kite -- 1.13 _+ 0.26 (7) ------1040 Goshawk 1.65 _+0.36 (50) 0.86 -+ 0.09 (44) -- -- 0.46 (1) 1110 Long-earedowl 2.10 (2) 0.98 -+ 0.28 (6) 0.84 (2) 1.93 (1) 0.75 (2) 270 2.83 (40) 0.87 (38) 0.78 (36) 1.94 (12) 0.42 (2) 310 Short-Pared owl 3.17 (2) 1.22 (2) 0.98 (1) 2.48 (1) 1.64 (1) 350 Tawnyowl 2.55 _ 0.19 (3) 0.71 -+ 0.10 (3) -- 1.91 (2) 1.26 _+0.38 (3) 460

liver, and kidney between eight speciesof Falconi- significant loss in tissue weight (Barton and Houston formes and four Strigiformes.We also examined 1992); we therefore discardedany birdswhich had obvi- ously lain for some time before being frozen. heart weight in thesespecies to see if this is heavier In order to test our hypothesis,we first needed to cat- in specieswith an energetic form of prey capture. egorize the predatory styleof each raptor species.For the Finally, we considered the correlation between Falconiformes we did this based on literature review of body condition and the size of these organs. the proportion of avianprey in each speciesdiet. Species taking more than 75% avian prey were categorizedas METHODS attackers and included peregrine falcons (Falcoperegn- Most of the birds used in this study had been found nus), sparrowhawks(Accipiter nisus), and goshawks(A. dead and sent to the Institute of TerrestrialEcology as a gentilis),while speciestaking predominantly small mam- part of their program to monitor pesticideresidues. In mals and carrion were categorizedas searchersand in- addition, a sampleof goshawkswas examined which had cluded buzzard (Buteo buteo), red kite (Milvus milvus), been shot under licensefor game preservationand im- and kestrel (Falco tinnunculus)(Brown1978). Attackers ported under license (CITES 038371A). Birds were were specieswhich capture prey by high-speed aerial stored frozen at -20øC for up to 6 wk. It is known that chase,requiring great accelerationand agilitywith an av- freezing has little effect on gut morphology, but pro- erage hunting successof 13% (TemPles1985). Searchers, longed periods between death and freezing can lead to however,were speciescapturing mammalian prey mainly

Table 2. Correlation betweenorgan size (g) and index of body condition of variousspecies of raptors.Sample sizes given in parentheses.

SPECIES SEX GIZZARD HEART

Sparrowhawk M r = 0.71, P= 0.0018 (16) r = 0.89, P= 0.02 (6) F r = 0.53, P= 0.0018 (32) r = 0.63, P= 0.02 (13) Peregrine M r = 0.96, P = 0.03 (4) r = 0.96, P = 0.01 (5) Kestrel M r = 0.55, P = 0.09 (10) -- F -- r = 0.80, P = 0.03 (7) Buzzard M r = 0.93, P = 0.0001 (10) r = 0.87, P= 0.0001 (16) F -- r = 0.77, P= 0.0003 (17) Red Kite M r = 0.69, P = 0.31 (4) r = 0.95, P = 0.004 (6) Goshawk M r = 0.33, P= 0.12 (23) r = 0.58, P= 0.002 (25) F r = 0.44, P = 0.07 (18) r = 0.79, P = 0.0001 (19) Barn Owl r = 0.34, P= 0.19 (16) r= 0.78, P= 0.02 (8) TawnyOwl -- r = 0.72, P = 0.28 (4) DECEMBER 1996 INTERNAL ORGAN SIZE IN RAPTORS 221 by dropping on it from above and not depending so and sternum diagonal length (from base of sternum to heavily on high-speedpowered flight, with higher rates distal point of coracoid) as the best predictors.We used of prey capture (Temeles 1985). For the owl speciesex- the product of these two measuresas our body sizefactor amined, the main difference in hunting strategybetween and used this factor as the covariatein ANCOVA analysis specieswas that barn ( Tytoalba) and long-earedowls to correct for body size differences.We log-transformed (Asiootus) have an active flight mode with prey mainly data on both axes. The Bonferroni method was used for located while in flight, while tawnyowls (Styixaluco) are pairwise comparison of adjusted treatment means (Day more passivepredators, locating prey from perch sites and Quinn 1989). (Cramp and Simmons 1980). Since our study dealt with evolutionary adaptation of There was some variation in the condition of the birds digestiveorgan size with relation to hunting strategy,we availablefor this study.We used dry weights to record considered including a phylogenetic component in our organ massbecause we did not know the extent to which analysis.However, since the speciessample was small and carcasseshad become dehydrated after death. Wet we had specieswith contrastinghunting strategiesin the weightswere used only from birds known to have died same genus,we decided there would be no advantageto accidentallyand whose carcasseswere collected shortly adding a phylogeneticcomponent. after death. To considerthe contribution that each organ makesto The proventriculus, gizzard, small intestine, liver, kid- total body mass,we used a smaller sample of fresh car- ney, and heart were dissectedfrom 583 carcasses.Stom- cassesto obtain wet weightsof liver, kidney,proventncu- achswere separatedinto the proventriculus,whose func- lus, gizzard, small intestine, and heart. The weight of uon is the production and releaseof gastricsecretions, each organ was calculatedas a percentageof total body and the gizzard, which provides mechanical digestion mass. and preliminary proteolysis(Duke 1986). The length and We dissectedthe pectoralismuscle from each carcass w•dth of the proventriculuswere measuredwhen laid flat After weighing,it was dried at 70øCto constantweight. to estimate internal surface area. All other organs were Larger specieshad 10 g samplesof muscle tissuedried, cleaned of mesenteryand fat bodies:the heart had the from which total muscle dry weight was estimated from chambersopened and any blood clots removed.All tis- the wet weight of the sample and total muscle. Subsam- sueswere then oven dried at 70øCto constantweight. pies were shown to be representativeof the whole mus- The combined weight of proventriculus and gizzard is cle. A condition index which accountedfor body size dif- here referred to as stomach, and the combined mass of ferenceswas then calculatedby regressingthe dry weight proventriculus,gizzard, and small intestine as gut. Fal- of the two pectoral musclesagainst the skeletalbody s•ze coniformeswere analyzedseparately by sex, becauseof measure and savingthe residuals.The variablesbeing ex- their , and sufficient data were avail- amined were standardizedin the same way, again sawng able to analyzemale and female sparrowhawks,peregrine the residuals. Correlations between the two sets of resid- falcons, kestrels, common buzzards, red kites, and gos- uals were then examined. hawksseparately. We used a skeletalbody sizevariable to correct for differencesin body sizebetween species (Bar- RESULTS ton and Houston 1994). We used Principal Components Analysis to identify Male and female sparrowhawksand goshawks which of the six body measureswere best predictors of had the lightest gizzardsand stomachsfor birds of body size, and identified the length of the sternum keel their size, while red kites and common buzzards (from base of the sternum to anterior edge of the keel) had the heaviest. Sparrowhawkshad the lightest small intestines and common buzzards and red

Table 2. Extended. kites the heaviest. When total mass of the gut was considered, the guts of the goshawk,sparrowhawk, and peregrine were the lightest for their body size and those of the kestrel and common buzzard the SMALL SMALL INTESTINE INTESTINE LENGTH DRY WEIGHT heaviest. All comparisons were significant (P < 0.05) with no significant heterogeneity in regres- r = 0.51, P = 0.009 (25) r = 0.45, P = 0.06 (18) sion slopes. In considering heart weight, there r = 0.06, P = 0.72 (39) r = 0.30 P: 0.07 (36) were significant differences among the speciesex- r = 0.14, P = 0.79 (6) r = 0.95 P-- 0.01 (5) r = 0.60 P = 0.12 (8) r = 0.89 P = 0.001 (9) amined, but these were not consistent. Among r = 0.15 P = 0.63 (13) r = 0.79 P= 0.0005 (15) males, kestrels had the largest heart relative to r= 0.60. P = 0.01 (17) r = 0.69 P= 0.0017 (18) body mass but, in females, goshawksand sparrow- r = 0.09 P-- 0.70 (22) r = 0.34 P-- 0.12 (22) hawks were heavier. r= 0.63. P = 0.18 (6) r = 0.99 P: 0.0001 (6) Among owls, the tawny owl had a significantly r = 0.09 P = 0.65 (25) r = 0.04 P = 0.83 (25) heavier proventriculus,small intestine, and total di- r= 0.35. P = 0.13 (20) r = 0.69 P = 0.001 (19) gestivetract than expected for a of this size. r = 0.28 P = 0.17 (24) r = 0.37 P= 0.14 (17) There were no significant differences in heart r = 0.99 P = 0.004 (4) r = 0.95 P = 0.05 (4) weight between owls. 222 N. BARTON AND D. HOUSTON VOL. 30, NO. 4

We were not able to obtain dry weights for liver waysbe the best measure of gut tissuebecause the and kidney tissuebut determined their wet weights alimentary tract can stretch, so that differencesin as a percentageof total bodyweight (Table 1). This length may not necessarilyreflect a corresponding was a lesssatisfactory method of indicating relative difference in tissue mass. Here we have shown that organ size becausebirds differed in their fat con- small intestine tissue weight also varies between tent, gut content, and overall muscle condition species,and that those specieswith an attacking making body weight a poor predictor of actual mode of predation have significantlyless intestine body size (Barton and Houston 1994). To mini- tissuethan those that do not depend so heavilyon mize this problem, we only included data from rapid accelerationfor prey capture.Apart from the birds which were freshly killed from accidental small intestine, the stomachsize is alsoimportant, causesand which seemedto be in good condition. for this not only involves the mass of the organ Sample sizeswere small but there is no indication itself, but also determines the weight of food that that liver,kidney, or heartmass was associated with a speciescan consume. We found that a species predatory strategy.Liver and kidney made up ap- such as the sparrowhawk which faces selection proximately the same proportion of body mass pressuresto minimize bodyweight doesshow small acrossall species.The largestrelative heart sizewas stomach mass. This may accentuate the impor- found in the peregrine and merlin (Falcocolumbar- tance of diet quality between raptors.We showed zus)both of which have high power output require- earlier (Barton and Houston 1993) that species ments. However, the goshawk and buzzard, two with short intestine lengths are lessefficient at di- specieswith directly contrastinghunting strategies, gestion and can only maintain body weight when had the same relative heart size. fed on prey speciesof high calorific value. If they Stomach sizewas variable. The kestrel had a very alsohave significantlysmaller stomachs,and so can large stomach for a bird of its size. Compared to consumea smaller amount of prey, the difference the sparrowhawk,the kestrel had a stomachthree in organ size emphasizesthe need to take prey of times larger. The relative size of the kestrel gut high energy content to compensatefor the lower more closely resembled that of the Strigiformes overall intake. In Strigiformes, proventriculusand suggestingit might be a dietary adaptationfor spe- small intestine weight (and also length, see Barton cies feeding largely on small . and Houston 1994) was greatest in the tawny owl We used weight of the pectoral muscle as an in- which is the specieswith the most passivehunting dex of body condition becausethis varies consid- mode compared to the barn owl or long-earedowl erably and is the largest muscle in the body of a (Barton and Houston 1994). bird. Individualswhich we categorizedsubjectively While there appears to be clear associationsbe- as having died of starvation had on average only tween predatory strategy and the total weight of 54% of lean dry pectoralmuscle weight compared the digestivetract, this is not the casefor the liver, to that found in individuals which had been killed kidney, and heart. The size of these organs seems by collisions.For all speciesthere wasa significant to be strictly determined by metabolic body size, positive correlation between condition and the and presumablycannot be reduced in masswith- weight of the small intestine (Table 2). The length out seriouslyimpairing tissuefunction and the fit- of the small intestinewas also positivelycorrelated ness of the bird. with condition in male sparrowhawks,male buz- The variations that are found with body condi- zards and tawny owls. Gizzard weight was also tion were perhaps to be expected. When found to be significantlycorrelated with body con- enter periodsof food deprivation,they depend on dition for sparrowhawks,male peregrines, and endogenousreserves of fat and protein to main- male common buzzards.Heart weight was highly tain their metabolic requirements. The extent to correlated with condition in every speciesexcept which tissuefrom the alimentary tract is depleted, the tawny owl. however,is little known. Our finding that species we examined showed very significant lossesof tis- DISCUSSION sue when in poor condition demonstratesthat gut In an earlier analysiswe showed that the length tissue is widely used as a reserve. Presumablyany of the smallintestine in raptorsvaried betweenspe- reduction in gut tissuehas a detrimental effect on cies and seemedto be stronglyassociated with the digestiveefficiency, and so birds do not experience predatory strategy.However, length might not al- this tissueloss unless they have no alternative. The DECEMBER 1996 INTERNAL ORGAN SIZE IN RAPTORS 223 finding that heart muscle is also significantlylost 1994. Morphological adaptation of the digestive in birds in poor condition also demonstratesthat tract in relation to feeding ecologyin raptors.jr. Zool. when birds reach poor body condition even the Lond. 232:133-150. most vital organs are affected. ,L.H. 1978. British birds of prey. Collins, Lon- don, UK. ACKNOWLEDGMENTS CP,AMP, S. AND K.E.L. SIMMONS. 1980. Handbook of the We are extremely grateful to Ian Wyllie and Ian New- birds of , the Middle East and North Al•ica. ton at the Institute of Terrestrial Ecology and to Steve The birds of the western Palearctic. Vol. 2. Oxford Petty at the Forestry Commissionfor providing most of University Press,Oxford, UK. the birds used for this study.The project was funded by DAY, R.W. AND G.P. QUINN. 1989. Comparisons of treat- a Natural Environment Research Council CASE Student- ments after an analysisof variance in ecology. Ecol. ship with the Nature ConservancyCouncil to N.W.H.B. Monog• 59:433-463. LITERATURE CITED DuRE,G.E. 1986. Alimentary canal:secretion and diges- B^RTON, N.W.H. ^ND D.C. HOUSTON. 1992. Post-mortem tion, special digestivefunctions and absorption. In changesin avian grossintestinal morphology. Can.J. P.D. Sturkie, Avian Physiology.Springer-Verlag, New Zool. 70:1849-1851. York, NY U.S.A. 1993a. The influence of gut morphologyon di- TEMELES,E.J. 1985. Sexual size dimorphism of bird-eat- gestiontime in raptors. Comp.Biochem. Physiol. A. 105: ing hawks: the effect of prey vulnerability. Am. Nat. 571-578. 125:485-499. 1993b. A comparison of digestiveefficiency in birds of prey. Ibis 135:363-371. Received 4 October 1995; accepted 26 August 1996