INFLUENCES
OF TIME POSTMORTEM,
DIET ON DIGESTIVE
TWO
ORGAN
FEEDING ACTIVITY,
MORPHOLOGY
AND
OF
EMBERIZIDS
ROBERT
J. ROBEL,
• MICHAELE. BARNES,
• KENNETHE. KEMP,2
AND JOHN L. ZIMMERMAN•
•Division
of Biology
and2Department
of Statistics,
Kansas
StateUniversity,
Manhattan, Kansas 66506 USA
ABSTRACT.--We
conducted
experiments
to determinethe effectof timepostmortem,
feeding
activity,and diet on changesin digestiveorganmorphologyin Dark-eyedJuncos(Junco
hyemalis)
and Harris' Sparrows(Zonotrichia
querula).
We measureddigestiveorgansimmediately,or at 30, 60, or 90 min postmortem,
but detectedno time-relateddifferences
in DarkeyedJuncos.
The smallintestinesof free-feedingDark-eyedJuncos
were longerthanthose
of food-deprived
birds.We foundno significantdiet-relateddifferences
in lengthsof small
intestines
of Harris'Sparrows.
Livermassreflectedenergyintakeof free-feeding
versusfooddeprivedHarris' Sparrows.Received
4 August1989,accepted
7 April 1990.
THE AVIAN literature abounds with descriptions of changesin digestive organ morphology. Researchers
attributed changesin avian gizzard size to the texture
and fiber content
(Zonotrichiaquerula)and the Dark-eyed Junco
(Juncohyemalis).
of the
METHODS
diet (Ziswiler and Farher 1972,Savoryand Gentle 1976a, Kehoe and Ankney 1985), and reported a relationship between gizzard massand
body mass in northern Galliformes (Thomas
1984, Moss 1983). Leopold (1953) and Kehoe
and Ankney (1985) suggestedthat a high-fiber
diet causesincreasedlengthsof smallintestines,
a conclusion reached by several researchers
working on tetraonids(Moss 1974, Pendergast
and Boag1973, Pulliainen and Tunkkari 1983).
A causal relationship between cecal size and
dietary fiber was proposed(Leopold 1953) and
supported with experimental evidence (Moss
1972, 1989;Savoryand Gentle 1976b;Mossand
Trenholm 1987;but see Remington 1989). Ziswiler and Farher (1972) contended that largeintestine length reflectsthe diet of avian species, and Savory and Gentle (1976a, b) could
produce increasesin large-intestine length by
adding fiber to the diet of JapaneseQuail (Coturnix coturnix).
Most pertinent reports on avian specieshave
involved gallinaceousbirds and waterfowl. Little attention has been focusedon changesin
gut morphologyof passerines,or the influence
of time postmortemor feeding activity on measurementsof gut morphology.In this study,we
examinedthe effectsof time postmortem,feeding activity, and diet on digestive organ morphology of two emberizids, Harris' Sparrow
669
Birdswere capturedduring winter near Manhattan,
Kansas.After capture,all birds were confinedindividually in 38 x 22 x 27-cm wire cagesand placed
in an environmental
chamber
under
constant
10øC
temperature, 10L:14D photoperiod,and 76-78% relative humidity. Water and a maintenancepelleted
mashdiet were providedadlibitumfor at least30 days
before any experimentation.Before and during experiments, we measuredmassto the nearest 0.01 g
within 15 min of the onsetof the light period. After
birdswere killed by cervicaldislocation,we measured
wing length (distancefrom proximal tip of carpometacarpusto tip of leading primary feather), and
determinedage (by skull ossification;Wiseman 1962)
and sex (by examination of gonads).
We removed the gastrointestinal tracts and associated organs from the carcasses,and discarded the
esophagus,proventriculus,and pancreas.The small
intestinewasisolatedby separationat the gizzardand
ileo-cecaljunctions.The cecawere disjoinedfrom the
small intestine, and the large intestine was considered
to be that portion from the ileo-cecaljunctionto and
including the cloaca. Lengths of ceca (both combined),smallintestine,and largeintestinewere measuredto the nearest1.0 mm usingLeopold'sstraight
ruler technique(FreehlingandMoore 1987).One person measuredthe lengths of all intestinesand ceca.
Wet masses(patted dry) of small intestine,large intestine,ceca(both combined),gizzard (without contents),and liver were recordedto the nearest0.1 mg.
After measuringand determinin$wet mass,we dried
intestinesand associated
organsat 65øCfor 24 h, and
The Auk 107: 669-677.
October
1990
670
ROBEL
ET^L.
determined their massagain to the nearest 0.1 mg.
Data were analyzed using analysisof variance (ANOVA) procedures,including ANOVA for repeated4 x
4 Latin Squares(Cochranand Cox 1962).Fisher'sprotectedleastsignificantdifference(LSD) (Oft 1984)was
usedfor pairwisecomparisons.The significancelevel
for all testswas P = 0.05; meansin the text are pre-
[Auk,Vol. 107
EXPERIMENT II
Feedingactivity.--Dark-eyed Juncos(n = 64) were
divided randomlyinto four 16-birdgroups,and each
was assignedrandomly to 4 x 4 Latin Squares.Birds
were not segregatedby sex or age. Water was pro-
vided ad libitumduring all trials. Free-feedingand
food-deprivationtrialswere conducted;eachusedtwo
The nutrientvalueof feedsusedin the experiments 16-bird groups. In food-deprivationtrials, we removed food from the cage at the onset of the phowas determinedby examining one sampleof eachby
proximateanalysis,moisturecontentby massloss,ash toperiodon the day birdswere to be killed; otherwise,
by igniting dried samplesat 600øC,crudefat by dieth- the balanced mash was provided ad libitum.In the
free-feeding trials, the balancedmash was provided
yl ether extraction (Cullison 1982),and crude protein
by the Kjeldahl method (Perry 1984). Residue re- ad hbitumthroughout.Fourbirds from eachtreatment
sented _+ SE.
maining after acidic and alkaline digestion was considered crude fiber (Nagy and Haufler 1980),and nitrogen-freeextractlessashwasthe remainingfraction
of the sample.Energy content was determined in an
adiabaticoxygenbomb calorimeter.
group were killed each day either at onset or 3, 6, or
9 h after the beginning of the light period.
We measured
the mass of each bird at the onset of
the light periodandwhen killed. Beforewe measured
the intestinesfor length, we purged them of food.
We
recorded
wet
masses of small
intestines
before
and after purging them. Measurementsof intestines
EXPERIMENT I
and associatedorganswere as describedabove.
The datafrom the four Latin Squareswere analyzed
Postmortem
changes.--Thirty-twoDark-eyed Juncos
by
analysisof varianceaspairsof repeated4 x 4 Latin
were divided into two 16-bird groups. One group
Squares.The model usedin the analysiswas
consisted of adult males, and the second contained
juvenile malesand femalesof unknown age. Wing
lengthwasusedto separateadult malesfrom females,
and to separatejuveniles from adults (Yunick 1981).
Each group was assignedrandomly to 4 x 4 Latin
Squares.The blocking factors(rows and columns)in
the Latin Squareswere groups of birds and day of
sacrifice,with day of sacrificebeing commonamong
squares.Water and a balanced mash were provided
ad lbitum during the experiment. Treatments consistedof killing specificbirds and evisceratingthem
immediatelyor at 30, 60, or 90 min after death.Four
birds from each group (8 birds) were killed at the
onsetof the light period eachday, and measurements
were made of digestive tractsand organs at predetermined postmortemtimes.
The data from the two Latin Squareswere analyzed
Y,jk•m
= I• -{-T• + S(.)j+ Dk + G(,)•+ Hm+ e,t•m,
where Yij•mis the responseobservedfor the ith feeding treatment, the jth squarewithin the ith feeding
treatment,the kth day, the/th group of birds within
the jth squareof the ith feeding treatmentand the
mth hour; • representsthe overall mean of the responsevariable; T, representsthe ith feeding treat-
ment-deprived
or full-fed;S(•)j
represents
the effectof
the ith squarewithin the jth feeding regime; D• representsthe kth day; G(,)•representsthe /th group of
4 birds that were sacrificedfrom the jth squareon
the ith treatment;H• representsthe mth hour at which
evaluationoccurredafter onsetof the photoperiod(0,
3, 6, or 9), and ei• representsthe randomerror as-
sociatedwith the i, j, k, l, and ruth observationand
as repeated4 x 4 Latin Squareswith day of sacrifice assumeddistributed N (0, a•).
commonbetweensquaresand groupsof birds nested
within squares.Thus the model was
EXPEPaMEN~r III
Y.jk•= t• + S, + G•o
• + Dk + T• + e•ik•,
Diet infiuences.--Harris'Sparrows(n = 35) that had
where Y•jk•
is the responseobservedin the ith square, been fed a balancedmashfor 30 daysin the environfor the jth group of birds, killed on the kth day, and mental chamber were divided randomly into four
meanof the responsevariable,S•representsthe effect
groups. Ten were fed sunflower (Helianthusannuus)
seeds,10 were fed white proso millet (Panicurnmili-
of the ith square of birds (adult male or mixed im-
aceurn)seeds, 10 were fed the balanced mash, and 5
evisceratedat the/th time, • represents the overall
maturesandfemales),G(,)•
represents
thejth randomly providedbaselineinformation. The 5-bird group was
assignedgroupof birdswithin the ith square,D• rep- killed on the first day of the trial, and pertinent mearesents the effect of the kth day, T• representsthe
surementswere made to characterizethe experimen-
effectof the/th timeat evisceration,
ande,• represents tal birds. Food (either sunflower seeds, millet seeds,
the random error associatedwith the /, j, k, and /th or mash)and water were provided ad libitum.Waterobservation and assumed to be distributed N (0,
solublevitamin and mineral supplementswere added
October
1990]
Time,
Feeding,
andGutMorphology
to the water of eachbird eachday to minimize dietary
deficienciesdue to single-seeddiets.
Five birds in eachof the 10-birdgroupswere main-
TABLE 1.
671
Selected nutritional
tainedon their respectivedietsfor 7 or 14days,then
killed. This yielded seven5-bird groups:I baseline
Characteristic
group,3 groupsfed differentfeedsfor 7 days,and 3
groupsfed differentfeedsfor 14 days.Carcassmass Energycontent(kJ.g •)a
wasdeterminedand wings measured,the birdswere Crudeprotein(%)
Ether extract(%)
eviscerated,and their digestivetract and organswere
Crude fiber (%)
measuredas describedpreviously.Food consumed
Ash (%)
was determinedby substractingspilled and uneaten Nitrogen-freeextract(%)
food from the amount provided each bird.
One-wayanalysisof variancewas usedto compare
the 7-treatmentgroupmeansfor the variablesof interest.In the caseswhere the F-testswere significant,
LSDswere usedto separatetreatment means.To comparefeedmain effects,the baselinegroupwasdropped
from the analysisand the remaining6 groupswere
comparedin a 3 x 2 factorialANOVA with the 3
typesof feedsconstitutingone factor,and time on
feed the other. The error mean square from the 7treatment
ANOVA
was used as the F-test denomi-
nator in the 3 x 2 factorial analysis.
RESULTS
The three foods used in the experiments varied
in
nutritional
characteristics.
Sunflower
seedshad the highest energy content and the
least fiber (Table 1). Millet seedshad twice the
fiber contentand approximately60%of the energy contentof sunflowerseeds(Table 1).
characteristics of the
three feeds.
Moisture (%)
Millet
Mash
Sunflower
seeds
seeds
19.3
24.9
19.7
11.4
31.4
25.7
1.6
4.5
6.8
4.2
6.5
3.8
56.1
3.1
3.3
62.2
74.1
11.8
12.5
12.9
6.3
All measurements
in dry mass,exceptfor moisturemeasurements.
data were pooled to determine effectsof time
postmortemon length and massof intestines
and associatedorgans.
Not one of the intestinelengthsor associated
organmasseswas significantlydifferentwhen
measuredimmediately or at 30, 60, or 90 min
after death (Table 2). The dry massto wet mass
ratios were fairly consistentover the 90-min
time period for small intestines(0.25:0.22),gizzards (0.30:0.29), and livers (0.30:0.29), but de-
creasedslightly with time for large intestines
(0.17:0.12).
Feedingactivity.--Initial massesof food-deprived (18.4 + 0.3 g) and free-feeding(18.5 _+
0.4g) birdsdid not differ,but 3 h afterthe onset
of the light period, the massof free-feeding
birds increasedto 20.2 + 0.6 g, which was sig-
DARK-EYEDJUNCOS
Postmortem
changes.--Cranialossificationwas
completein somefemales;therefore,we could
notagefemalesaccurately.
Wing lengthsof adult
males(80.6 + 0.4 mm) were significantlylonger
than thoseof juvenile males(75.3 + 0.8 mm)
and unknown aged females (75.1 + 0.5 mm).
The bodymassof adult males(19.1 + 0.3 g) was
nificantlygreaterthan the 17.9+ 0.2 g of fooddeprived birds. By hour 9, the massof freefeeding birds was 20.4 + 0.4 g, significantly
more than the 16.5 + 0.3 g of food-deprived
birds.
There was no significant difference in the
lengthsof small intestinesof free-feedingand
food-deprivedbirds at the start of the light period, but from the third hour on, the lengths of
significantly
greaterthanin juvenilemales(17.8 the small intestine of free-feeding birds were
+ 0.4 g) and unknownagedfemales(17.8 + 0.5 significantly longer than those of food-deg). Exceptfor dry cecalmasses,we detectedno prived birds (Table 3, Fig. 1). Wet massesof
differencesin length or massof intestines or smallintestinesof food-deprivedbirdsand those
associated
organsamongadult males,juvenile
of small intestines
males, or females of unknown age. Dry cecal
massof adult males(2.2 + 0.1 mg) and females
feedingbirdsdid not changeor differ with time.
After 3 h into the light period, however, each
without
contents
of free-
of unknownage(2.0 + 0.2mg)wassignificantly was significantlylighter than wet massesof
heavierthan that of juvenile males(1.6 + 0.2 small intestines with contents. We observed no
in dry masses
of the small
mg). Becauseof the lack of differencesamong significantdifferences
intestines from free-feeding or food-deprived
birds
throughout the 9-h experiment.
amongage/sexgroups(exceptdry cecalmass),
measurements
of birds of different
mass and
672
ROBEL
aTAL.
180
[Auk, Vol. 107
free-feeding birds were significantly greater
than those of food-deprived birds 9 h after the
onsetof the light period (Table 3).
Lengths and wet massesof ceca from freefeeding and food-deprived birds did not differ
during the 9-h experiment.Dry mass,however,
of cecaof free-feeding birds was greater than
that of food-deprivedbirds throughout the experiment (Table 3). No significant differences
were detectedin the wet or dry massesof giz-
170
160
150
zards (Table 3).
130
0
TIME
3
(h) AFTER
6
ONSET
9
OF LIGHT
PERIOD
Fig. 1. Mean (n = 8) lengths of small intestines
from free-feeding (closedcircles)and food-deprived
(opencircles)Dark-eyedJuncoskilled at varioustimes
after onset of the light period. Vertical lines extend
+1
SE.
Although liver wet massesof food-deprived
and free-feeding birds were not significantly
different at the start of the experiment,they
declined during the experiment for food-deprived birdsand increasedfor free-feedingbirds
(Fig. 1). Liver wet masswas significantlyheavier in free-feeding birds from the third hour
onward(Table3). An identicalpatternof change
was observedin dry massesof livers (Table 3).
No significantchangesoccurredin the lengths HARRIS' SPARROWS
or wet massesof large intestinesof free-feeding
and food-deprivedbirds.The dry massesof large
Dietinfluences.--At
the startof this 14-dayexintestines of free-feeding and food-deprived periment,wing lengthsof birdsassignedto each
birds did not differ at the start of the experi- diet did not differ. Initial masses of the three
ment,but the dry masses
of largeintestinesfrom diet groups did not differ significantly. Birds
TABLE2. Mean (+SE) wing lengths (mm), body masses(g), and digestive organ lengths (mm) and masses
(mg) from Dark-eyedJuncos(n = 8) taken at selectedtimespostmortem.
Parameter
Wing length
Bodymass
Small
Time
postmortem
(min)
0
77.3 + 1.2ß
18.7 + 0.4
Experimental
30
60
90
77.6 + 1.1
18.1 + 0.6
78.7 + 1.1
18.0 + 0.6
77.9 + 1.2
19.0 + 0.6
SE
1.1
0.5
intestine
Length
142.1 + 2.1
140.2 + 3.1
138.5 + 3.6
143.3 + 3.0
Wet mass
650.0 + 34.3
653.8 + 51.2
585.0 + 27.4
637.5 + 50.1
Dry mass
159.7 + 8.3
147.5 + 13.9
129.1 + 5.9
141.3 + 8.9
3.0
40.8
9.3
Large intestine
Length
13.6 + 1.4
12.0 + 1.0
13.2 + 1.5
15.1 + 1.0
1.2
Wet mass
40.0 + 3.8
40.0 + 6.0
36.2 + 5.0
43.8 + 5.0
4.9
Dry mass
6.8 + 0.6
5.4 + 0.4
4.7 + 0.8
5.4 + 0.5
0.5
5.1 + 0.4
2.2 + 0.2
5.8 + 0.3
2.1 + 0.2
5.3 + 0.7
1.9 + 0.2
6.5 + 0.5
2.1 + 0.2
0.5
0.2
Wet mass
582.5 + 22.4
613.8 + 23.1
582.5 + 28.0
606.3 + 17.4
Dry mass
174.6 + 7.6
175.8 + 10.3
165.9 + 8.9
176.5+ 6.9
Wet mass
637.5 + 29.7
757.5 + 50.1
750.0 + 29.1
746.3 + 36.2
36.3
Dry mass
190.3 + 8.1
218.5 + 16.0
212.6 + 6.0
216.9 + 12.9
10.8
Ceca (combined)
Length
Dry mass
Gizzard
22.7
8.4
Liver
Meanswithin a row are not significantlydifferent(P = 0.05).
October
1990]
Time,
Feeding,
andGutMorphology
673
T^I•I,E3. Mean(+SE) lengths(ram)andmasses
(rag)of digestiveorgansfromfree-feedingandfood-deprived
Dark-eyedJuncos(n = 8) killed at varioustimesafteronsetof the light period.
Experi-
Time (h) after onsetof light period
Measurement
0
3
Small
6
9
mental
SE
Intestine
Length
Food-deprived
Free-feeding
144.1+ 3.4Aa
142.9+ 2.2A
139.8+ 3.5A
160.4+ 2.6C
139.5+ 3.8A
157.6+ 3.6C
135.3+ 2.0B
170.3+ 2.7D
Food-deprived
608.7+ 27.9A
624.4+ 32.3A
542.7___
31.1A
501.9+ 32.7A
Free-feeding
(minus contents
Free-feeding
512.8 + 49.6A
553.5 + 31.9A
494.9 + 65.6A
562.4 + 97.1A
(with contents)
512.8 + 49.6A
1,035.3+ 43.9B
938.1 + 65.2B
1,101.7+ 51.9B
Wet
3.0
mass
64.8
Dry mass
Food-deprived
Free-feeding
Length
Food-deprived
Free-feeding
Wet
158.1+ 9.4
128.7 + 12.4
160.1+ 6.3
127.1+ 6.6
162.5 + 21.0
151.0 + 18.3
Large Intestine
129.5+ 7.1
176.6 + 23.1
8.5 + 0.7
9.3 + 0.8
9.0 --- 1.0
8.5 + 0.6
8.8 + 0.6
10.8 + 0.8
9.3 + 1.0
11.1 + 0.7
27.2 + 2.2
20.8 + 1.6
25.4 + 2.3
25.5 + 1.1
21.5 + 3.2
18.7 + 1.4
21.0 + 2.8
23.2 + 2.9
13.0
0.8
mass
Food-deprived
Free-feeding
2.2
Dry mass
Food-deprived
Free-feeding
6.1 + 0.6AB
4.8 + 0.2BC
6.2 + 0.6AB
7.3 + 0.4A
5.5 + 0.7BC
6.3 + 0.5AB
4.3 + 0.7C
7.2 + 0.7A
0.6
Ceca (combined)
Length
Food-deprived
Free-feeding
5.5 + 0.5
6.0 + 0.4
5.3 + 0.5
6.8 + 0.5
6.0 --- 0.5
6.6 + 0.8
5.6 + 0.6
6.1 + 0.4
0.5
5.3 + 0.9
6.4 + 0.8
5.8 + 0.8
6.5 + 0.6
4.6 + 0.6
6.6 + 0.8
5.0 + 0.8
5.3 + 0.8
0.8
1.3 + 0.1A
1.8 + 0.2BC
1.6 + 0.1ABC
1.8 + 0.1BC
1.5 + 0.3AB
1.9 + 0.1C
1.3 + 0.1A
1.6 + 0.1C
0.1
23.9
Wet mass
Food-deprived
Free-feeding
Dry mass
Food-deprived
Free-feeding
Gizzard
Wet
mass
Food-deprived
Free-feeding
Dry mass
Food-deprived
Free-feeding
640.1 + 29.8
599.1 + 13.8
588.5 + 20.0
591.7 + 26.3
572.4 + 19.9
612.8 ___22.9
580.0 + 35.3
601.4 ___24.4
181.2 + 7.9
171.9 + 4.5
169.2 + 6.0
166.8 ___7.7
171.2 + 10.7
163.0 + 7.1
172.5 ___6.6
174.1 + 7.0
7.2
Liver
Wet
mass
Food-deprived
Free-feeding
655.1 + 28.8AB
684.0 + 28.8AB
708.3 ___
43.8A
890.7 + 53.9D
569.2 + 18.2BC
920.2 + 63.5D
204.5 + 9.8AB
211.7+ 7.6A
217.3 + 15.0A
285.8+ 19.4C
177.0+ 6.0B
327.9+ 25.1D
533.1 + 29.3C
1,054.4+ 42.9E
38.6
166.4 ___
6.2B
382.2+ 15.5E
13.1
Dry mass
Food-deprived
Free-feeding
ßMeansunletteredor with the sameletter,comparedbothhorizontallybetweenhoursand verticallybetweenfeedingregimesfor the same
digestiveorgan,are not significantlydifferent(P • 0.05).
674
ROBSL
STAL.
[Auk, Vol. 107
TABI•S
4. Mean (+SE) lengths (ram) and masses(rag) of small intestines,large intestines,and combinedceca
from Harris' Sparrows(n = 5) fed 1 of 3 feedsfor 7 or 14 days.
Mass
Day/food
Length
Small
Wet
Dry
Intestine
Day 0
Mash
170.0 + 2.3'
966.9 + 60.6
126.6 + 7.4
177.8 + 5.4
173.0 + 6.7
168.6 + 4.5
1,097.2 + 47.9
1,025.1 + 71.4
1,100.2 + 48.4
114.3 + 5.5
107.4 + 10.3
101.2 + 9.2
172.4 + 4.9
1,082.0 + 61.4
114.2 + 10.6
Day 7
Mash
Millet
Sunflower
Day 14
Mash
Millet
Sunflower
Experimental SE
164.6 + 1.9
915.1
+ 53.7
98.6 + 4.9
181.0 + 9.2
1,154.1 + 58.4
107.5 + 10.6
5.0
57.5
8.5
Large Intestine
Day 0
Mash
14.0 + 1.2
44.4 + 3.2
6.6 + 0.5
15.5 + 1.3
15.8 + 2.1
14.0 + 1.3
53.1 + 6.7
48.1 + 5.1
44.3 + 5.1
6.7 + 0.5
6.0 + 0.8
6.1 + 0.5
14.2 + 1.6
15.3 + 1.0
43.3 + 5.9
46.9 + 8.5
4.9 + 0.6
6.0 + 0.4
14.4 + 1.3
57.7
7.0 + 0.8
Day 7
Mash b
Millet
Sunflower
Day 14
Mash
Millet b
Sunflower
Experimental SE
1.4
+ 2.4
5.3
0.6
Ceca (combined)
Day 0
Mash
Mash b
6.8 + 0.7
6.5 + 0.3
5.1 + 1.1
5.2 + 0.9
1.5 + 0.3
1.4 + 0.2
6.6 + 0.2
6.6 + 0.3
5.1 + 1.3
5.2 + 0.9
1.6 + 0.3
1.4 + 0.2
7.2 + 0.2
7.0 + 0.3
6.6 + 0.4
4.7 + 0.9
4.2 + 0.2
4.5 + 0.5
1.3 + 0.1
1.3 + 0.1
1.3 + 0.1
0.8
0.2
Day 7
Millet
Sunflower
Day 14
Mash
Millet
Sunflower
ExperimentalSE
0.3
Meanswithin a column for a specificorgan are not significantlydifferent (P = 0.05).
consumed9.97 + 0.81 g of mash per day, significantly more than millet (7.00 + 0.38 g). Both
values were significantly greater than the 4.92
+ 0.20 g of sunflowerseedsconsumedper day.
On the seventhday of the experiment,none of
the bird groupshad gained or lost a significant
amount of mass.At the end of the 14-day experiment, birds fed millet had lost an average
of 2.2 + 0.9 g, and thosefed balancedmashhad
lost an averageof 0.9 +__
0.2 g. Birds fed sunflower seeds,however, had gained an average
of 0.3 +--0.8 g.
Neither length nor mass of small or large
intestines or combined ceca was changed sig-
nificantly by diets (Table 4). Gizzard massof
birds on different diets varied during the 14dayexperiment(Table5). No significantchanges
were detectedin gizzard massesof birds on the
October
1990]
Time,
Feeding,
andGutMorphology
675
TABLœ
5. Mean(+SE)masses
of gizzards
andliversfromHarris'Sparrows
(n= 5) provided
1 of 3 feedsfor
7 or 14 days.
Gizzard mass
Day/food
Wet
Liver mass
Dry
Wet
Dry
Day 0
Mash
969.9 + 29.0Ba
283.6 + 7.7B
1,209.4 + 43.2AB
369.5 + 14.3AB
Day 7
Mash
Millet
949.5 + 28.4AB
890.2 + 30.4A
274.1 + 5.6AB
262.1 + 13.4A
1,301.1 + 125.9AB
1,177.6 + 126.0ABC
399.1 + 26.6B
362.1 + 36.7ABC
1,054.1+ 12.4BC
316.3+ 7.0BC
Mash
1,016.4+ 57.8BC
292.4+ 17.5BC
Millet
927.1 _+56.3AB
267.0 + 17.3AB
949.4 + 87.3CD
326.8+ 17.0C
1,073.3+ 50.9BCD
Sunflower
875.3+ 43.3D
271.9+ 13.9D
1,340.7+ 97.6A
414.3 + 25.8B
Day 14
Sunflower
1,134.7+ 62.9C
Experimental
SE
39.6
10.8
82.0
299.4 + 22.2CD
324.8+ 16.5BCD
22.3
ßMeanswith the sameletterwithin a columnare not significantly
different(P = 0.05).
mash diet.
Gizzard
masses of birds
on millet
decreasedsignificantlyby the seventhday, but
by the fourteenthday they were similar to the
originalmass.Gizzardsfrombirdsfed sunflower seedsincreasedsignificantlyin massduring
the 14-day experiment (Table 5). Exceptfor a
significantseventhday decreasein liver masses
of birds provided sunflowerseeds,no diet-related trendswere noted in wet or dry liver masses of Harris' Sparrows.
DISCUSSION
We found a lack of age- and sex-relateddifferencesin digestiveorganmorphologyin wintering Dark-eyedJuncos,which is consistent
with reports of Gier and Grounds(1944) on
HouseSparrows(Passer
domesticus),
Kirkpatrick
(1944)on Ring-neckedPheasants
(Phasianus
colchicus),and Leopold (1953) on California Quail
(Callipepla
californica).
The practiceof pooling
aviandigestiveorganmassandlengthdataappearsjustifiedif they arecollectedduringnonbreeding periods. We believe that measurements of digestiveorgan morphologycan be
recordedup to 90 min postmortem--orperhaps
longer--without lossof accuracy.However, if
histologicalinformationis required,measurementsand fixationshouldbe done immediately
after death to avoid autolysis(Fenwick 1982).
Although we measuredseveralorgansof avi-
an digestive tracts, we will concentrateon
changesof the small intestinebecauseit constitutesapproximately85%of the length of the
emberiziddigestivetract,and it servesasa pri-
marysitefor digestionin mostbirds.We noted
few significantchangesin size of cecaor gizzardsin either species.Liver massesincreased
in free-feedingbirds during the 9-h period in
Experiment
II, anddecreased
in birdsprovided
millet in ExperimentIII; both presumablyreflect changesof storedliver glycogen.
The effectsof food consumptionon small intestine length could explain someof the con-
tradictoryresultsof changesin digestiveorgan
morphologyreportedin the literature.We did
not attemptto separatetime effectsfrom food
consumptioneffects.We believe effectof time
of day on small-intestinelength was minimal,
because small-intestine lengths of food-de-
prived birds did not changeduring the 9-h
experiment.The lengthsof smallintestinesof
free-feedingbirds after initial feeding (except
between hours 6 and 9) were also unchanged.
Birdsin the free-feedingmode began feeding
at the onsetof the light period and continued
to feed throughout the light period.
Changesin small-intestinelength in birds
during winter are commonly attributed to
changesin diet, specifically
an increasein fibrouscontent (Davis 1961;Moss 1972, 1974;Pulliainen and Tunkkari 1983). However, no
changewasreportedin small-intestine
lengths
in Ring-neckedPheasants
(Kirkpatrick1944)or
SageGrouse
(Centrocercus
urophasianus;
Huppand
Braun1984)in spring,when low-fiberfood replaceshigh-fiber food in the diet. Our results
may shedlight on this apparentinconsistency.
During winter, many nonmigratorybirds in
temperatezones are forced to consumefood
676
ROnEL
•r AL.
continuouslyto meet energy needs. Presumably the digestive tracts of these birds are distendedthroughoutthe day. In lessstressfulperiods, most birds feed only in early mornings
and late evenings,and their intestinal tractsare
distended only during those periods. If bird
collectionsare madewithout regardto feeding
patterns,biasesin measurementsof gut length
can result. For example,continuouslyfeeding
birds (free-feedingin ExperimentII) collected
[Auk,Vol. 107
patterns,and that the digestivetract contents
be removed
before measurements
ACKNOWLEDGMENTS
This study was supportedby the National Science
Foundation (Grant No. DEB-8022568), the Division of
Biology,KansasStateUniversity, and the KansasAgricultural Experiment Station. This is Contribution
No. 90-8-Jfrom the KansasAgricultural Experiment
Station,KansasState University.
in late morningor early afternoonwould have
elongatedintestinal tracts.In the samebirds on
an early-morning-and-late-afternoonfeeding
regime, the intestinal tracts would not be distended at midday. Someof the autumn to winter changesin lengths of intestinal tracts reported in the literature could reflect such
differencesin feeding patterns.
Savoryand Gentle (1976a)reported lengtheningof smallintestinesof Japanese
Quailwhen
fiber was added to the diet. Although the fibrous content
are made.
LITERATURE CITED
COCHRAN,
W. G., & G. M. COX. 1962. Experimental
designs,2nd ed. New York, J. Wiley & Sons.
CULLISO•,I,
A. E. 1982. Feeds and feeding, 3rd ed.
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DAVIS,J. 1961. Some seasonalchangesin the morphologyof the Rufous-sidedTowhee.Condor 63:
313-321.
FELL,B. F. 1969. Morphology of the absorptivesurfacesof the alimentary tract. Pp. 295-344 in Nutrition of animalsof agriculturalimportance.Part
of the three feeds we used varied
1: The science of nutrition of farm livestock (D.
Cuthbertson, Ed.). Oxford, Pergammon Press.
by a factor of 2, we detected no changesin
B.W. 1982. Light and scanningelectron
intestinal length related to fiber content. In- FENWlCK,
microscopeevaluationof collectionmethodsused
creasedfiber in foods is commonly accompain preservationof canine intestine. M.S. thesis,
nied by a decreasein energy content,a situation
Manhattan, Kansas State Univ.
that could causechangesin avian feeding patFREEHLING,
M.D. & J. MOORE. 1987. A comparison
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of 2 techniquesfor measuringintestinal length.
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to feed more frequently, the observed gut GIER,L. J., & O. GROUNDS.1944. Histological study
lengthening could have been enhanced by
of the digestivesystemof the EnglishSparrow.
measurements
were
filled
with
taken when
the small intestines
Auk
61: 241-243.
food.
Hu??, J. W., & C. E. BRAUN. 1984. Spring changesin
lipid reservesof adult male SageGrouse.J. ColThe amount of food consumed may cause
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changesin gut size (Fell 1969,Pulliainen 1976,
and Pulliainen and Tunkkari 1983). In our ex-
periments,birds consumed12 g of mash,7 g of
millet, or 5 g of sunflowerseedsper day. If only
the quantity of food consumedcausedgut size
change, the birds on mash should have developed longer intestinal tractsthan birds on millet or sunflower. We detectedno such changes
in Harris' Sparrows.
We support the widely held belief that
changesin dietary fiber content alter the morphology of avian digestivesystems.Whether or
not our results can be extended to other passefinespeciesis unknown. The presenceof food
in the small intestinereflectedfeeding activity
patterns,and appearedto be an important factor
in observedchangesin small-intestinelength.
We recommendthat studiesof avian digestive
morphology consider avian feeding activity
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ducks (Aythya spp.). Can. J. Zool. 63: 2339-2342.
KIRKPATRICK,
C. M. 1944. Body weights and organ
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LEO?OLD,
A. S. 1953. Intestinal morphology of gallinaceous birds in relation to food habits. J. Wildl.
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Moss, R. 1972. Effectsof captivity on gut lengths in
Red Grouse.J. Wildl. Manage. 36: 99-104.
--.
1974. Winter diets, gut lengths, and interspecificcompetition in Alaskan ptarmigan. Auk
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1983. Gut size, body weight, and digestion
of winter foodsby grouseand ptarmigan.Condor
85: 185-193.
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1989. Gut sizeand the digestionof fiberous
diets by tetraonid birds. J. Exp. Zool. Suppl. 3:
61-65.
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gestibilityand gut sizein RedGrouse.Br. Poult.
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C. J.,& M. J.GENTLE.1976a. Effectsof dietary
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anddataanalysis,2nd ed.Bostonß
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in Alberta.
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PERRY,
T. W. 1984. Animal life-cycle feeding and
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&
. 1976b. Changesin foodintakeand
gut size in JapaneseQuail in responseto manip-
ulationof dietaryfibercontent.Br.Poult.Sci.17:
571-580.
THOMAS,V.G. 1984. Winter diet and intestinal pro-
portions of Rock and Willow ptarmigan and
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Inland Bird Banding 40: 47-52.
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P•JLL•A•NEN,
E. 1976. Smallintestineand caecalengths
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Lapland. Ann. Zool. Fennici 13: 195-199.
ZISWILER,
V., & D. $. FARNER.1972. Digestion and
ß& P. TUNKKARI.1983. Seasonalchangesin
the digestivesystem.Pp. 343-430 in Avian biolthe gut length of the Willow Grouse (Lagopus
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Suppl. 3: 87-94.
TheFrankM. ChapmanMemorialFundgivesgrantsin aidofornithological
research
andalsopostdoctoral
fellowships.
Whilethereisnorestriction
onwhomayapplyß
theCommittee
particularly
welcomes
andfavors
applications
fromgraduatestudents;
projects
in gamemanagement
andthemedicalsciences
areseldomfunded.
Applications
arereviewedoncea yearandmustbesubmittedno laterthan15January,with all supporting
material.Applicationformsmaybe obtainedfrom the Frank M. ChapmanMemorial Fund Committee,
Departmentof Ornithology,AmericanMuseumof NaturalHistory,CentralParkWestat 79thStreet,New
York, NY 10024-5192 USA.
Threepostdoctoral
fellowships
were awardedfor the 1989year:Jean-Louis
Martin,Aviangeographic
variationandspeciation
in thePalearctic:
Aretheregeneralrules?RichardO. Prum,Phylogenyandbehavioral
diversification
of the cotingas(Cotingidae);
and C. JefferyWoodbury,A taxonomicstudyof the avianspinal
cord.
Threecollection
studygrantsfor the 1989yearwereawarded:
TimothyCroweß
for a studyof supra-generic
phylogenetic
relationships
within thegamebirds
(Order:Galliformes);
NedraKleinßfor a studyof speciation
in the Yellow Warbler(Dendroica
petechia);
and Miguel LentinoRosciano,
for a studyof the systematics
of
Crypturellus
erythropus
and Tyto alba.
Chapmangrantsfor 1988,totaling$40ß066ß
with a meanof $598ßwere awarded:CraigW. Benkman,The
ecologyand statusof the HispaniolanCrossbill;William L. Bennet,How doesHouseFinchcolorvariation
affectfemalechoice?
James
V. Briskie,Dynamics
andconsequences
of copulation
patternsin Smith'sLongspurs;
KevinJ.Burns,Thegeography
of FoxSparrowontogeny;
AliceL. E. V. Cassidyß
Songvariationandlearning
in SongSparrows(Melospiza
melodia);
LuisM. Chiappe,Continentalbirdsfromthe LateCretaceous
of Patagonia;Carla CiceroßStuctureand variationin the songof the Lincoln'sSparrow(Melospiza
lincolnii)in
California;David A. Cimprich,Effectof flockingwith dominantheterospecifics
on nutritionalstatus;Evan
G. Cooch,Effectof growthrate on adultbody sizeand fecundityin SnowGeese;BarbaraDiehi, Structure
and functioningof a bird communityin a patchyand changinghabitat;AndreaDinep, The developmentof
socialbehaviorin White Ibis chicks;Keith L. Dixon, Investigationof the CrestedTitmousehybrid zone in
Texas;David Eastzer,Allozymefrequencies
acrossa songtransitionzone;ScottV. Edwardsß
Molecularevolutionin cooperatively
breedingAustralo-Papuan
babblers(Pomatostomus);
BruceA. Eichhorst,
Geneticvariation in the Westernand Clark's grebes:color-morphsor species?Lisa M. Ellis, Interactionof testosterone
anddelayedplumagematurationin Black-headed
Grosbeaks;
DavidEnstrom,Matechoiceanddelayedplumagematuration
in OrchardOrioles;PatriciaEscalante,
Evolutionary
relationships
of Geothlypis
warblers;
Charles
M. FrancisßSurvival ratesof LesserSnow Geese;ReneeD. Godard,Individual discriminationby two wood
(continuedon p. 736)