Download factors influencing the size of some internal organs in raptors

j RaptorRes.30(4):219-223
¸ 1996 The Raptor ResearchFoundation, Inc.
FACTORS
INFLUENCING
NIGEL
THE SIZE OF
IN RAPTORS
W. BARTON AND DAVID
SOME
INTERNAL
ORGANS
C. HOUSTON
AppliedOrnithology
Unit, DivisionofEvolutionaryand Environmental
Biology,GrahamKerr Building, Universityof
Glasgow,
Glasgow,G12 8Q• Scotland
ABSTP•CT.--Thesize of the small intestine, stomach,kidney, liver and heart were compared among
raptor speciesand consideredin relation to hunting strategyand body size. Speciesrelying on rapid
accelerationand maneuverability
to capturepreyin flight,suchassparrowhawk
(Accipiter
nisus),goshawk
(A. gentilis),and peregrine (Falcoperegrinus),
had the smallestdigestivetracts for their size. Species
dependingmore on soaringflight which do not need fastaccelerationto captureprey,suchascommon
buzzard (Buteobuteo),red kite (Milvus milvus), and European kestrel (Falco tinnunculus),had heavy
digestiveorgans.In the Strigiformes,the same relationshipwasfound, and specieswhich hunt by active
flight, such as barn owl (Tyt0 alba), and 1ong-earedowl (Asiootus),had significantlylighter digestive
tracts than the tawny owl (Strix aluco),a specieswhich mainly hunts from a perch dropping onto its
prey from above.Body condition waspositivelycorrelatedwith organ weights,including the heart, but
to a lesserextent with linear measuresof size such as intestine length.
KEYWOe.DS: internalorgans;predatorybirds;condition.
Factoresque infiuencian el tamafio de algunos6rganosinternos en rapaces
RESUMEN.--EItamafio del intestinodelgado,est6mago,riffones,higado y coraz6n,rue comparadoentre
especiesde rapacesque difieren en estrategiade caza y tamafio corporal. Especiesbasadasen r•pida
aceleraci6ny maniobrabilidadpara capturarpresasen vuelo, talescomoAccipiter
nisus,A. gentilis
y Falco
peregrinus
ten/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,talescomo Buteobuteo,
Milvus
milvusy Falcotinnunculus,tenlan 6rganosdigestivosm:ispesados.En Strigiformesse encontr6 la misma
relaci6n, especiesque cazanpor vuelo activo,tales como Tytoalba,Asiootus,ten/an un tracto digestivo
significativamentem•s liviano que Atrix aluco,una especieque caza esperandoa la presa desde una
percha.La condici6ncorporalestuvocorrelacionadapositivamentecon el pesode los 6rganos,incluyendo el coraz6n.
[Traducci6n de Ivan Lazo]
We previouslyreported that birds of prey show
considerablevariation in the length of their small
intestines (Barton and Houston 1994) and suggestedthat these differencescould be due to adaptationsfor different stylesof predation. We hypothesized that raptors which capture prey by
pouncing on it from abovewould have the longest
gut lengths for efficient digestion while species
which need to acceleraterapidly to capture active
prey, such as predatorstaking small prey in flight,
would have very light organ systemsto enable
them to acceleratemore rapidly. Reductionin the
length of the small intestine probablyresultsin less
efficient absorption of food but this could still be
selected for if this disadvantagewere more than
compensatedfor by a higher rate of prey capture.
We were
able to demonstrate
that there
was an as-
219
sociation between the length of the small intestine
and the predatory strategyshownby a species,and
that after correcting for differences in body size,
those species that specialized in the capture of
small birds in flight had smallintestinallengthsup
to 50% shorterthan specieswith a lessactivepredatory style. The small intestine is responsiblefor
nutrient absorption and is therefore the organ
most likely to effect absorptionefficiency.We have
shown that specieswith short small intestines digest their food less efficiently, and as a consequence select only prey items of high energy content (Barton and Houston 1993a, 1993b).
This paper considerswhether there may be associations between predatory strategy and the
weight of other organ systems.We compared the
massof the gizzard, proventriculus,small intestine,
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 combinationof the sizesof internal organsof both sexesand samplesizesare given
in parentheses.
SMALL
SPECIES
Kestrel
Merlin
Sparrowhawk
Peregrine
Buzzard
Red Kite
Goshawk
Long-earedowl
Barn owl
Short-Pared owl
Tawnyowl
LWER
HEART
3.24 -+ 0.46 (14) 1.13 -+ 0.14 (12)
3.24 -+ 0.84 (3)
2.20 +- 0.31 (3)
2.63 -+ 0.53 (86) 1.12 +_0.14 (75)
2.76 +_0.43 (3) 1.81 _+0.05 (3)
2.15 +_0.47 (5) 0.86 +_0.15 (31)
-1.13 _+ 0.26 (7)
1.65 _+0.36 (50) 0.86 -+ 0.09 (44)
2.10
(2) 0.98 -+ 0.28 (6)
2.83
(40) 0.87
(38)
3.17
(2)
1.22
(2)
2.55 _ 0.19 (3) 0.71 -+ 0.10 (3)
KIDNEY
1.14_+ 0.22
1.1o
0.81 ___
0.12
0.86_+0.2
0.92 +_0.05
--0.84
0.78
0.98
--
STOMACH
(10)
(1)
(59)
(3)
(3)
2.62 +- 0.34
1.56 ___
0.32
0.95 -+ 0.13
1.24
1.48 _+0.41
(12)
(3)
(38)
(1)
(4)
0.75
0.56
0.63
0.53
0.99
--
M_ASS
_+0.42 (18)
(1)
_+0.28 (22)
+_0.05 (3)
_+2.62 (7)
--
-(2)
(36)
(1)
BODY
INTESTINE
1.93
1.94
(1)
(12)
2.48
1.91
(1)
(2)
0.46
0.75
0.42
1.64
1.26 _+0.38
180
190
220
760
850
1040
(1)
(2)
(2)
(1)
(3)
1110
270
310
350
460
significant loss in tissue weight (Barton and Houston
1992); we therefore discardedany birdswhich had obviouslylain for some time before being frozen.
In order to test our hypothesis,we first needed to categorize the predatory styleof each raptor species.For the
liver, and kidney between eight speciesof Falconiformes and four Strigiformes.We also examined
heart weight in thesespeciesto seeif this is heavier
in specieswith an energetic form of prey capture.
Finally, we considered the correlation between
body condition and the size of these organs.
Falconiformes
we did this based on literature
review
of
the proportion of avianprey in each speciesdiet. Species
taking more than 75% avian prey were categorizedas
attackers and included peregrine falcons (Falcoperegnnus), sparrowhawks(Accipiternisus),and goshawks(A.
gentilis),while speciestaking predominantly small mammals and carrion were categorizedas searchersand in-
METHODS
Most of the birds used in this studyhad been found
dead and sent to the Institute of TerrestrialEcologyasa
part of their program to monitor pesticideresidues.In
addition, a sampleof goshawks
wasexaminedwhich had
been shot under licensefor game preservationand imported under license (CITES 038371A). Birds were
stored frozen at -20øC for up to 6 wk. It is known that
freezing has little effect on gut morphology, but prolonged periods betweendeath and freezing can lead to
cluded buzzard (Buteo buteo), red kite (Milvus milvus),
and kestrel (Falco tinnunculus)(Brown1978). Attackers
were specieswhich capture prey by high-speedaerial
chase,requiring great accelerationand agilitywith an averagehunting success
of 13% (TemPles1985). Searchers,
however,were speciescapturingmammalianprey mainly
Table 2. Correlation betweenorgan size (g) and index of body condition of variousspeciesof raptors.Samplesizes
given in parentheses.
SPECIES
SEX
Sparrowhawk
M
r = 0.71, P= 0.0018 (16)
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
F
M
F
M
M
F
r = 0.55, P =
-r = 0.93, P =
-r = 0.69, P =
r = 0.33, P=
r = 0.44, P =
r = 0.34, P=
r=
r=
r=
r=
r=
r=
r=
Buzzard
Red Kite
Goshawk
Barn Owl
TawnyOwl
GIZZARD
--
HEART
r = 0.89, P= 0.02 (6)
0.09 (10)
0.0001 (10)
0.31
0.12
0.07
0.19
(4)
(23)
(18)
(16)
-0.80, P =
0.87, P=
0.77, P=
0.95, P =
0.58, P=
0.79, P =
0.78, P=
0.03 (7)
0.0001 (16)
0.0003 (17)
0.004 (6)
0.002 (25)
0.0001 (19)
0.02 (8)
r = 0.72, P = 0.28 (4)
DECEMBER 1996
INTERNAL ORGAN SIZE IN RAPTORS
by dropping on it from above and not depending so
heavilyon high-speedpowered flight, with higher rates
of prey capture (Temeles 1985). For the owl speciesexamined, the main difference in hunting strategybetween
specieswasthat barn owls( Tytoalba)and long-earedowls
(Asiootus)have an active flight mode with prey mainly
locatedwhile in flight, while tawnyowls (Styixaluco)are
more passivepredators, locating prey from perch sites
(Cramp and Simmons 1980).
221
and sternum diagonal length (from base of sternum to
distal point of coracoid) as the best predictors.We used
the product of thesetwo measuresas our body sizefactor
and used this factor as the covariatein ANCOVA analysis
to correct for body size differences.We log-transformed
data on both
axes. The
Bonferroni
method
was used for
pairwise comparison of adjusted treatment means (Day
and Quinn 1989).
Since our study dealt with evolutionary adaptation of
There was some variation in the condition
of the birds
digestiveorgan sizewith relation to hunting strategy,we
availablefor this study.We used dry weightsto record considered including a phylogenetic component in our
organ massbecausewe did not know the extent to which analysis.However,sincethe speciessamplewassmalland
carcasseshad become dehydrated after death. Wet we had specieswith contrastinghunting strategiesin the
weightswere used only from birds known to have died samegenus,we decided there would be no advantageto
accidentallyand whose carcasses
were 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 carney, and heart were dissectedfrom 583 carcasses.
Stom- cassesto obtain wet weightsof liver, kidney,proventncuachswere separatedinto the proventriculus,whosefunc- lus, gizzard, small intestine, and heart. The weight of
uon is the production and releaseof gastricsecretions, each organ wascalculatedas a percentageof total body
and the gizzard, which provides mechanical digestion mass.
We dissectedthe pectoralismusclefrom each carcass
and preliminary proteolysis(Duke 1986). The length and
w•dth of the proventriculuswere measuredwhen laid flat After weighing,it wasdried at 70øCto constantweight.
to estimate internal surface area. All other organswere 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. Subsamsueswere then oven dried at 70øCto constantweight. pies were shown to be representativeof the whole musThe combined weight of proventriculus and gizzard is cle. A condition index which accountedfor body sizedifhere referred to as stomach, and the combined mass of
ferenceswasthen calculatedby regressingthe dry weight
proventriculus,gizzard, and small intestine as gut. Fal- of the two pectoral musclesagainstthe skeletalbody s•ze
coniformeswere analyzedseparatelyby sex, becauseof measureand savingthe residuals.The variablesbeing extheir sexual dimorphism, and sufficientdata 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 residfalcons, kestrels, common buzzards,red kites, and gos- uals were then examined.
hawksseparately.We useda skeletalbody sizevariableto
correct for differencesin body sizebetweenspecies(Bar- RESULTS
ton and Houston 1994).
We used Principal Components Analysis to identify
which of the six body measureswere best predictors of
body size, and identified the length of the sternum keel
(from base of the sternum to anterior edge of the keel)
Male and female sparrowhawksand goshawks
had the lightestgizzardsand stomachsfor birds of
their size, while red kites and common
small
Table
2.
SMALL
SMALL INTESTINE
LENGTH
r = 0.51, P = 0.009 (25)
r = 0.06, P = 0.72 (39)
r = 0.14, P = 0.79 (6)
r = 0.60
P=
r = 0.15 P =
r= 0.60. P =
r = 0.09 P-r= 0.63. P =
r = 0.09 P =
r= 0.35. P =
0.12
0.63
0.01
0.70
0.18
0.65
0.13
intestines
and
common
buzzards
and
red
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
Extended.
INTESTINE
buzzards
had the heaviest. Sparrowhawkshad the lightest
(8)
(13)
(17)
(22)
(6)
(25)
(20)
DRY WEIGHT
r = 0.45, P = 0.06 (18)
r = 0.30 P: 0.07 (36)
r=
r=
r=
r=
r=
r=
r=
r=
0.95
0.89
0.79
0.69
0.34
0.99
0.04
0.69
P-- 0.01 (5)
P = 0.001 (9)
P= 0.0005 (15)
P= 0.0017 (18)
P-P:
P=
P=
0.12 (22)
0.0001 (6)
0.83 (25)
0.001 (19)
r = 0.28
P = 0.17 (24)
r = 0.37 P= 0.14 (17)
r = 0.99
P = 0.004 (4)
r = 0.95 P = 0.05 (4)
and those of the kestrel
and common
buzzard
the
heaviest. All comparisons were significant (P <
0.05) with no significant heterogeneity in regression slopes. In considering heart weight, there
were significant differences among the speciesexamined, but these were not consistent. Among
males, kestrels had the largest heart relative to
body massbut, in females, goshawksand sparrowhawks
were
heavier.
Among owls, the tawny owl had a significantly
heavierproventriculus,smallintestine,and total digestivetract than expected for a bird of this size.
There were no significant differences in heart
weight between owls.
222
N. BARTON AND D. HOUSTON
We were not able to obtain dry weights for liver
and kidney tissuebut determined their wet weights
asa percentageof total bodyweight (Table 1). This
wasa lesssatisfactorymethod of indicating relative
organ size becausebirds differed in their fat content, gut content, and overall muscle condition
making body weight a poor predictor of actual
body size (Barton and Houston 1994). To minimize this problem, we only included data from
birds which were freshly killed from accidental
causesand which seemedto be in good condition.
Sample sizeswere small but there is no indication
VOL. 30, NO. 4
waysbe the best measure of gut tissuebecausethe
alimentary tract can stretch, so that differencesin
length may not necessarilyreflect a corresponding
difference
in tissue mass. Here
we have shown that
small intestine tissue weight also varies between
species,and that those specieswith an attacking
mode of predation have significantlylessintestine
tissuethan those that do not depend so heavilyon
rapid accelerationfor prey capture.Apart from the
small intestine, the stomachsizeis alsoimportant,
for this not only involves the mass of the organ
itself, but also determines the weight of food that
thatliver,kidney,or heartmasswasassociated
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 doesshowsmall
acrossall species.The largestrelativeheart sizewas stomach mass. This may accentuate the imporfound in the peregrine and merlin (Falcocolumbar- tance of diet quality between raptors.We showed
zus)both of which havehigh power output require- earlier (Barton and Houston 1993) that species
ments. However, the goshawk and buzzard, two with short intestine lengths are lessefficient at dispecieswith directlycontrastinghunting strategies, gestion and can only maintain body weight when
had the same relative heart size.
fed on prey speciesof high calorificvalue. If they
Stomachsizewasvariable. 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
and Houston 1994) was greatest in the tawny owl
cies feeding largely on small mammals.
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 appearsto be clear associations
beas having died of starvationhad on averageonly tween predatory strategyand the total weight of
54% of lean dry pectoralmuscleweightcompared 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 organsseems
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 masswithweight of the small intestine (Table 2). The length out seriouslyimpairing tissuefunction and the fitof the small intestinewasalsopositivelycorrelated ness of the bird.
with condition in male sparrowhawks,male buzThe variations that are found with body condizards and tawny owls. Gizzard weight was also tion were perhaps to be expected.When animals
found to be significantlycorrelated with body con- enter periodsof food deprivation,they depend on
dition for sparrowhawks,male peregrines, and endogenousreservesof fat and protein to mainmale 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 showedvery significantlossesof tisDISCUSSION
sue when in poor condition demonstratesthat gut
In an earlier analysiswe showedthat the length tissueis widely used as a reserve. Presumablyany
of the smallintestinein raptorsvaried betweenspe- reduction in gut tissuehas a detrimental effect on
cies and seemedto be stronglyassociatedwith the digestiveefficiency,and so birds do not experience
predatory strategy.However, length might not al- this tissuelossunless they have no alternative. The
DECEMBER 1996
INTERNAL ORGAN SIZE IN RAPTORS
finding that heart muscle is also significantlylost
in birds in poor condition also demonstratesthat
when birds reach poor body condition even the
most vital organs are affected.
ACKNOWLEDGMENTS
We are extremely grateful to Ian Wyllie and Ian Newton at the Institute of Terrestrial Ecology and to Steve
Petty at the Forestry Commissionfor providing most of
the birds used for this study.The project was funded by
a Natural
Environment
Research
Council
CASE Student-
ship with the Nature ConservancyCouncil to N.W.H.B.
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Received4 October 1995; accepted 26 August 1996