The Auk 111(1):170-177, 1994
SUCROSE
INTOLERANCE
DIAGNOSTIC
IN BIRDS: SIMPLE
NONLETHAL
METHODS AND CONSEQUENCES FOR
ASSIMILATION
OF COMPLEX
CARBOHYDRATES
HYLARY L. MALCARNEY, CARLOS MARTINEZ DEL RIO,
AND VICTOR
APANIUS
Departmentof EcologyandEvolutionary
Biology,PrincetonUniversity,
Princeton,New Jersey08544, USA
ABSTR^CT.--Gray
Catbirds(Dumetella
carolinensis,
Mimidae) and Purple-headedGlossy-Starlings (Larnprotornis
purpureiceps,
Sturnidae)showeddepressedingestionand increasedfecal
sugar contentswhen shifted from glucoseand fructoseto sucrosesolutions.These species
alsoexhibitedno increasesin plasmaglucoseafter ingestionof sucrose,but an increasein
plasmaglucoseafter ingestionof equicaloricdosesof a mixtureof glucoseand fructose.In
vitromeasurements
of intestinaldisaccharidase
activitiesin D. carolinensis
revealedinsignificantsucrase
activity,and low levelsof maltaseactivities.Theseresultssupportthe hypothesis
that sucroseintoleranceis a shared-derivedcharacterof the monophyleticlineagethat includesstarlings, mimids, and thrushes,and indicate that sucroseintolerance in birds can be
easilydiagnosedwith a combinationof behavioraland nonlethalphysiological
measurements. We suggestthat, in birds, low intestinal maltaseactivity is correlatedwith the lack
of sucraseactivity. We further hypothesizethat sucrose-intolerant
birds are poor at assimi-
lating complexcarbohydrates.
Received
I March1993,accepted
17November
1993.
PROXIMATE
NUTRIENT
ANALYSIS
distinguishes carbohydrate compositions.Nectar and fruit
between two broad classesof carbohydrates: pulp contain sucrose,glucose, and fructose in
structuralcarbohydrates,largely composedof varying proportions(Bakerand Baker 1983,Bafi-l,4 polysaccharideslike cellulose,and soluble ker et al. 1993). The chemical differences becarbohydratesincluding toorio- and disaccha- tween thesesugarsare relatively small. Sucrose
rides and a-l,4 and a-l,6 polysaccharides
like is a disaccharideof glucoseand fructose,and
glucoseand fructosediffer
starch,amylopectin,and glycogen(Whistlerand the monosaccharides
Daniel 1985). Most vertebrateshave endoge- only in the position of the carbonyl group. To
nousenzymesthat canhydrolyzethe a linkages be assimilated, sucrosehas first to be hydroin starchand glycogen,but do not possess
en- lyzed into its components--glucoseand fruczymes capableof breaking the fi linkages of rose--by the intestinalenzyme sucrase.Glucose
cellulose and hemicellulose (Vonk and Western and fructoseare absorbeddirectly by the intes1984). Vertebrates that assimilate the structural
tine (Alpers 1987). Some frugivorous birds lack
carbohydratecomponentin food have to rely intestinal sucraseactivity and cannot split the
on time consuming microbial fermentation
sucrose
bondbetweenglucoseand fructose(e.g.
Martinez del Rio and Stevens 1989). For these
species,sucroseis a uselessenergy source that
whereassolublecarbohydratesare considered can cause osmotic diarrhea and a consequent
(Stevens 1988). Structural carbohydratesare
generally considered "hard" to assimilate
"easy" to assimilate (Prop and Vulink 1992).
Here we presentdata showing that this pattern
has exceptions and that some soluble carbo-
hydratesmay be extremelydifficult or impossible to assimilateby a broadgroup of birds.
Martinez del Rio et al. (1992) demonstrated
that even
subtle differences
in the chemical
structureof solublecarbohydratescan result in
differences in bird digestive-utilization efficiency,in preferencesamongthesesubstances,
and presumablyin differential utilization by
birdsof foodplantscontainingdifferentsoluble
170
feeding aversion (Brugger and Nelms 1991).
Thesesamesucrose-intolerant
birds avidly ingest and profit from glucoseand fructose.
Martinez del Rio (1990)reportedthat sucrase
is lacking in severalspeciesof birds in the families Sturnidae (starlings) and Muscicapidae
(thrushes).DNA-DNA hybridization data suggestthat thesefamiliesare part of a monophyletic lineage (Sibley and Ahlquist 1990).These
dataalsosuggestthat membersof the Mimidae
(catbirds,mockingbirdsand thrashers)are the
closestliving relatives of starlings(Sibley and
January1994]
Sucrose
Intolerance
in Birds
Ahlquist 1984, 1990). Martinez del Rio (1990)
hypothesized that lack of sucraseis a sharedderived trait of the monophyletic lineage that
includes starlings, thrushes, and catbirds (the
sturnid-muscicapidlineage sensu Sibley and
Ahlquist 1990). Here we explore behavioral and
physiologicalcorrelatesof sucroseingestion in
two speciesof fruit-eating birds in this lineage:
Gray Catbirds (Dumetellacarolinensis,
Mimidae)
and Purple-headed Glossy-Starlings(Lamprotornispurpureiceps,
Sturnidae).Basedon the phylogeneticaffinitiesof GrayCatbirdsand PurpleheadedGlossy-Starlings,
we predictedthat they
would: (1) lackintestinalsucraseactivity;(2) be
unable to assimilatesucrose;and (3) reject sucrosein feeding trials.
cose. This
latter
171
method
is a modification
of a test
commonly used to diagnosedisaccharideintolerance
in humans (Isokosi et al. 1972, Krasilnikoff et al. 1975).
We validated thesemethodsin D. carolinensis
by measuring the activity of intestinal disaccharides(including sucrase)in vitro.
Dumetella carolinensis(mean mass
36.3 + SD of
4.0 g, n - 9) are among the most frugivorous birds in
temperate North America (Martin et al. 1951, Bent
1948).The fractionof fruit in Gray Catbird dietscan
be as high as 95% during the fall and winter (Beal
1897,Blake and Loiselle 1992),and is reducedonly
during the breeding seasonwhen they becomemainly insectivorous(White and Stiles 1990, Helmy and
Martinez del Rio unpubl. data).Lamprotornis
purpureiceps(meanmass= 79.4 + 10.6g, n = 4) are gregarious
forest birds widely distributed in West and Central
Africa (Nigeria, Gabon,Central African Republic,and
Maltose and isomaltose are the most abunUganda;Mackworth-Praed
and Grant1955,Sibleyand
dant productsof the hydrolysis of starch by Monroe 1990). Their diet apparently also consists
salivaryand pancreaticamylases.Maltoseis hy- largely of fruit (Beecher 1978, Serle et al. 1977).
We captured eight immature D. carolinensis
with
drolyzedby two independentenzymesystems:
sucrase-isomaltase
and maltase-glucoamylase mist nets in early October 1991 at the Hutchinson
(Semenza and Auricchio 1989). Becausesucrase- Memorial Forest,New Jersey,and at a secondaryfield
isomaltaseis a powerful maltase,its deficiency adjacentto the Sourland Mountain State Park, New
Jersey(birdsagedfollowingSuthersand Suthers1990).
in humans is often associated with reduced abilFour L. purpureiceps
(two malesand two females)were
ity to utilize dietary starch(Auricchioet al. 1963, obtained on loan from the Bronx Zoo. Birds were
1972). Isomaltaseis hydrolyzed by sucrase-iso- individually housedin 48 x 48 x 48 cm cagesat 21øC
maltase,and to a small degree by maltase-glu- and on a 12L/12D daily cycle. Food and water were
coamylase.Martinez del Rio (1990) suggested
that birds lacking intestinal sucrasealsowould
be poor hydrolyzers of maltose.We predicted
that, if sucraseactivity were low or missingin
D. carolinensis,both maltase and isomaltase ac-
tivity would be low.
MATERIALS
Sucrose
intolerance
AND METHODS
in vertebrates
is most
com-
monly causedby the absenceof intestinal sucrase
activity (Gudman-Hoyer et al. 1984). Measuring sucraseactivity requires biochemical analysis of intestinal tissue (Dahlqvist 1984). Obtaining samples of
intestinaltissuesfrom live smallbirdsis not yet practical and, consequently, measuring sucraseactivity
requires sacrificingbirds and extracting the intestine
(Martinez del Rio 1990). To diagnose sucroseintolerance in D. carolinensis
and L. purpureiceps,
we used
two nonlethaland minimally invasivemethods.The
first method relies on sequentially feeding birds a 1:1
mixture of glucose and fructose, and then offering
them
sucrose. Sucrose-intolerant
birds
should
show
depressedingestion and increasedfecal sugar contents when shifted from glucoseand fructoseto sucrose. The second method involves measuring the
increasein plasmaglucoseafter birds have been challenged with an oral dose of sucrose.Sucrose-intolerant birds should show nil increasesin plasmaglu-
supplied ad libitumexcept during experiments. Birds
were fed a mixed diet of Ziegler soft-billed bird diet
(Ziegler Bros. Inc, Gardners,Pennsylvania)and banana mash (a mixture of mashed ripe bananas,vegetableoil, soyprotein isolatecomplementedwith methionine, and a vitamin supplement in an agar-based
gel; Denslow et al. 1987). All experiments were conducted from October 1991 to February 1992. At the
end of the experiments,L. purpureiceps
individuals
were returned to the Bronx Zoo. The surviving D.
carolinensis
individuals were releasedin August 1992.
We conducted
all behavioral
tests at the onset of
the light period (0800 EST). In each trial we removed
food and water, and lined the bottom of the cages
with teflon-coatedplastic to facilitate excreta collection.
Each test consisted
of four
2-h trials
conducted
in four successivedays. We offered birds sugar solutions in glass tubes consisting of an upper 42-cm
section and a lower 7-cm section bent upward at a 45ø
angle. Birds drank from an elliptical hole (2 x 1.5
cm) at the distal end of the lower portion of the tube.
In the first two trials we presented birds with a tube
containing a 1:1 mixture of glucoseand fructose(15%
mass/totalvolume). On days3 and 4, birds were presented with an equicaloric solution of sucrose.At the
end
of each trial
we measured
the amount
of test
solution consumed and collected 5 to 10 samples of
excreta from the bottom of each cage. We measured
fecal sugar from these samples with a temperature
172
MALCARNEY,
MARTINEZ
DELRIO,ANDAPANIUS
[Auk,Vol. 111
compensatedrefractometer (Reichter-Jung10431). 250 ml 1.0 M Tris/HC1, pH 7, plus 250 ml 0.5 NaH2PO;/Na2HPO4,pH 7). Glucosestandards(0-120 •g
in 200 •1 0.1 M sodium maleate buffer, pH 7) were
reacted with the stop develop reagent to obtain a
Although uratesand fecal materialscan make refractometer readings irmacurate, the refractive index of
bird fecal samplesprovides a consistentrelative indicatorof sugarexcretion(Martinez del Rio et al. 1989,
standard
Bruggerand Nelms 1991).We reportfecalsugarcon-
mogenateswas measuredusing the Bio-Radkit (Bio-
centration in percent of sucrose(Brix = massof sugar
per volume of solution; Bolten et al. 1979).
We measuredthe responsein plasmaglucoselevels
(PGL) in birdssubjectto two treatments:a 1:1glucose:
Rad, Richmond, California) with bovine serum al-
fructose intubation, and a sucrose intubation. Birds
were fastedovernight and intubated with 3 g/kg of
a 15%(mass/volume) sugar solution. After 30 min we
obtained approximately 200 •1 of blood by jugular
venipuncture using a 0.5-ml syringe with a 28-gauge
needle (Hoysak and Weatherhead 1991).We obtained
a blood sampleafter 30 min becausepreliminary data
indicated that plasmaglucosepeaksbetween 25 and
35 min after a 1:1 glucose:fructose challenge (see
Martinez del Rio et al. 1988:fig. 3). Bloodwas transferred to chilled heparinizedmicrocapillarytubesand
centrifuged for 5 min (IEC microhematocrit centrifuge; seeCohen 1966).We measuredplasmaglucose
after color development (Glucose-Trinder 500 reagent, Sigma Chemical Co.) on a spectrophotometer
curve.
Protein
in tissue ho-
bumin standards.To allow comparisonwith other
intestinal
disaccharidase
studies we calculated
disac-
charidaseactivities using three different standardization procedures:activity per unit intestinal area as
•mol.(min) '.(cm 2nominal area) •; activity per gram
of protein as •mol.(min) '.(cm2.gram of protein) ';
and total hydrolyric capacityas •mol.(min) •
Statisticalanalysis.--Althoughwe report descriptive
statisticsfor both speciesin all experiments,we only
report significance values from inferential statistics
testsfor data on D. carolinensis
for which samplesize
was adequate (eight individuals). The number of individuals of L. purpureiceps
studiedwas too small (four
individuals) to allow use of inferential statistics. For
paired data we usedsign tests,which are robustalbeit
conservative (Mosteller and Tukey 1977). To estimate
parametersof linear regressionswe used standard
least-squaresmethods. Results are given as œ-+ SD.
(Beckman DU-64) set at 505 nm. As an estimate of the
responseto a glucose:fructose or sucrosechallenge
we used the difference
concentration
RESULTS
in PGL 30 rain after treatment
and PGL in untreated birds fastedovernight. Because
Neither D. carolinensisnor L. purpureiceps
we were concernedabout stressingbirds excessively changed consumption of glucose and fructose
by repeatedly drawing blood in a short time, we ob-
solution from day 1 to day 2 (P > 0.I; Fig. I).
Consumption decreased in all individuals of
fasting PGL remains relatively constant at the tem- both speciesfrom day 2 to day 3, when birds
poral scaleof our experiments(three weeks;Martinez were shifted from glucoseand fructoseto sudel Rio and Phillips unpubl. data).Plasmaosmolarity crose (P < 0.05). This decline in consumption
was measured on a Wescor 5500 vapor pressureos- continued from day 3 to day 4 in all birds but
mometer.
one glossy-starling,which drank very little of
Three D. carolinensis individuals
were euthanized
the sucrosesolution during either days (P <
with a halothane
overdose. The small intestine was
0.05, Fig. 1). Fecal sugar levels over the fourimmediately excised,divided into three sectionsof day trials followed a similar pattern in both
equal length, and placed in ice-cold saline (1.02%).
species(Fig. I). Fecalsugarremainedlow (<2%
We slit eachsectionlongitudinally and measuredits
length and width to obtain an estimate of intestinal BRIX) the first two days of the trials (Fig. I),
nominal area.After weighing, eachsectionwasstored increasedon day 3 when birds were shifted to
in liquid nitrogen. We measuredsucrase,maltase,and sucrosesolutions(P < 0.05),and remainedhigh
isomaltaseactivitiesin theseintestinalsamplesusing through day 4 (P > 0.I, Fig. 1). These results
a previouslydescribedmethod(Martinez del Rio et suggesthigh assimilation of glucose and fructained a single fasting plasmameasurementper individual. This procedureis justified becausein birds
al. 1988)from Dahlqvist(1984).Martinez del Rio (1990)
provided details of the disaccharideassay.Briefly,
tissueswere homogenized in 350 mM mannitol in 1
mM Hepes/KOH, pH 7.5 (30 sat OMNI 5000 homogenizer setting6), and tissuehomogenates(100 •1) were
incubatedat 40øC(Prinzinger et al. 1991)with 100 •1
of 56 mM sugar (sucrose,maltose, and isomaltase)
solutionsin 0.1 M maleate/NaOH buffer, pH 6.5 for
10 min. After incubation,reactionswere arrestedby
adding 3 ml of a stop/develop reagent (one bottle of
Glucose-Trinder500 reagent[SigmaChemicalCo.] in
tose, but low assimilation
of sucrose.
We found the extremelybroad range of concentrationsof fastingplasmaglucosethat seems
to be typical of bird species(Hazelwood 1984,
Groscolasand Rodriguez1981,Marsh et al. 1984).
Fastingplasmaglucoseranged from 260 to 335
rag/100 ml in L. purpureiceps,
and from 287 to
458 rag/100 ml in D. carolinensis
(Fig. 2). All
individuals
showed
increased
PGL
relative
to
fasting levels 30 min after administration of
January 1994]
Sucrose
Intolerancein Birds
173
20
20-
15./•
Days
1and
2:
glucose
+fructose 15•
s3 and4 : s
•
10.
10 •
5.
5
O-
0
1
2
3
4
1
2
Days
3
4
Days
Fig. 1. Ingestionof glucose:fructose(days1 and 2) and sucrose(days3 and 4) solutions(open symbols)
and feca!sugarconcentrationafter ingestion(closedsymbols)in D. carolinensis
(circles)and L. purpureiceps
individuals(triangles).Solutionsof glucose:fructoseand sucrosewere equicaioric(15%mass/totalvolume).
glucoseand fructose(Fig. 2; P < 0.05). The mean
increasesabovefastinglevels in L. purpureiceps
and D. carolinensis were 104.9 + 19.2 and 191 +
18.2 rag/100 ml, respectively.In D. carolinensis
the increase in PGL over fasting levels after
administration with glucoseand fructosewas
linearly and negatively correlatedwith fasting
542
ß
Y=X
492'
PGL (Y = 350.9 - 0.7X; r = 0.77, P < 0.005),
ß
ß
suggestingregulation of maximal plasmaglucoseconcentration. As expected for sucrose-intolerant animals, none of the birds intubated
with sucroseshowed increased PGL (Fig. 2).
Surprisingly, all D. carolinensisindividuals
showed a small (-18.4 ñ 3.2 mg/100 ml) but
significant (sign test, P < 0.05) decreasein PGL
30 min after intubation with sucrose(Fig. 2).
392'
OA•
0
342 '
292 '
øø
Plasma osmolarity did not vary significantly
among treatments (P > 0.05). Mean plasma osmolarities for L. purpureiceps
and D. carolinensis
were 385.2 + 28.3 and 350.8 + 8.4 mg/100 ml,
respectively.
We found maltase and isomaltase activities
242'
A
2;8
3•8
3;8
4•8
45'8
FastingPlasmaGlucose(mg/100ml)
in
Fig. 2. Plasmaglucoseconcentrationafter 30 min
three D. carolinensis
individuals,but only traces
of sucraseactivity in two individuals and no
detectablesucraseactivity in another(Table 1).
Sucraseactivity was extremely low (less than
0.001 g of sucrose hydrolyzed-h '.individual •). Martinez del Rio (1990)reportedthat maltasewas linearly and positively correlatedwith
sucraseactivity in a sampleof 11 speciesof pas-
30 min after a glucose:fructosedose was 481 + 14
mg/100 ml and is representedby horizontal dotted
line. Identicalline (Y = X) denotingnoposttreatment
changein PGL relativeto fastinglevelsis shownas
serine birds. As predicted, mean maltaseactiv-
reference.
of glucose:
fructose
(closed
symbols)
andsucrose
(open
symbols)oral doses(3 g/kg in a 15%solution).Circles
representD. carolinensis
and trianglesL. purpureiceps
individuals.For D. carolinensis,
meanplasmaglucose
174
MALCARNEY,
MARTINEZ
DELRIO,ANDAPANIUS
[Auk,Vol. 111
TABLE1. Intestinal disaccharidaseactivities in three individuals of Dumetellacarolinensis
(ϖ SD). Disac-
charidases
measuredby glucoseliberatedafter incubatingtissuehomogenates
with 0.28M substrateat 40øC
for
10 min.
Maltase
Isomaltase
Sucrase •
Total activity
Activity/area
(•mol.min •)
(•mol.min •-cm 2)
28.96 ñ 14.12
0.29 + 0.12
0.04 ñ 0.05
2.38 + 0.88
0.02 ñ 0.01
0.004 + 0.001
Activity/mg of protein
(•mol.min t.g of protein
102.03 _+ 31.03
2.77 + 1.81
0.50 + 0.43
Only two individualsshoweddetectablesucraseactivity.
ity standardizedper unit nominal area of intestine ([total maltose hydrolysis]/[total small
purpureicepsand D. carolinensisare sucrose in-
intestine normal area]) in D. carolinensis
was low
intoleranceis causedby the absenceof signif-
tolerant, and indicate that in D. carolinensis this
the 95% confidence interval of the
icant intestinal sucraseactivity. The behavioral,
intercept of the maltase-versus-sucrase
regres- fecal sugar,and blood testsappear to be easy
nonlethaltechniquesto diagnosepoor sucrose
sion line for these 11 species(Fig. 3).
and within
digestion in birds. Care must be exercised in
the interpretation of behavioral testsand fecal
sugar tests,however. Birds that possesssucrase
DISCUSSION
In analogywith human clinical terminology,
activity but that are relatively inefficientat di-
gesting sucrose,suchas Cedar Waxwings (Bomcombination of symptoms including sucrose bycillacedrorum),can show sucroseaversion and
realabsorptionasevidencedby high fecalsugar increasedfecal sugarconcentrationwhen exfood (Martinez del
concentration, aversion to sucrosein sequential posedto sucrose-containing
feeding trials, and a "flat" responsein plasma Rio et al. 1989,K. E. Bruggerunpubl. data).Apglucoseafter sucroseingestion(Gudman-Hoyer parently, a reduction in consumption after exwe define
"sucrose
intolerance"
in birds
as a
et al. 1984). Our results demonstrate that L.
posure to sucroseaccompaniedby increased fe-
cal sugar concentration can be reliably
interpreted ascausedby inefficient digestionof
•
16
• 10
o
sucrose,but not necessarilyasevidence for lack
of intestinal sucraseactivity. Table 2 summarizes sugar fecal output in five speciesof sucrose-fedbirds, including Cedar Waxwings.Fecal sugarin thesespeciesvariesrelatively little
and does not differ significantly between species lacking sucraseand Cedar Waxwings
= 1.65, P > 0.2), which digest sucroseinefficiently (Martinez del Rio et al. 1989).
Why do thesefive speciesexhibit suchsimilar
fecal concentrations
when
fed on sucrose? As-
sumingthat all fecalsolutesare undigestedsucrose and transforming BRIX% to osmolarity
yields a mean fecal osmolarityequal to 380 _+
15 raM. This value is slightly higher than the
Sucrase
Activity
(]amol
.min
'•.cm'2)
averagevalue for passerineplasmaosmolarity
Fig. 3. Linear regression (thick line) and 95% con(342 + 18.5 raM; Skadhauge1981). Birds with
fidenceintervals(thin lines) for relationshipbetween
poor or no digestionof sucroseare apparently
intestinal sucraseand maltaseactivitiesin 11 species
of passerinebirds(open circles).Relationshipexclud- incapable of concentratingexcreta against a
ing D. carolinensis
is Y = 1.4 + 7.4X; r = 0.95; Martinez
del Rio 1990).Closedsymbolrepresents
averagevalues for D. carolinensis
(from Table 1). Error bars are
SE. Note that point for D. carolinensisis within the
95% confidenceinterval for passefineregression.
concentration gradient to osmolarities much
higher than plasma(see Skadhauge1981:92).
Because
plasmaosmolarityisvery similaramong
smallpasserinespecies,fecalsugarafter sucrose
ingestionshouldalsobe similar.A corollaryof
January
1994]
Sucrose
Intolerance
inBirds
175
TABLE2. Comparisonof fecal sugar in sucrose-fedGray Catbirds (Dumetellacarolinensis),
Purple-headed
Glossy-Starlings(Larnprotornis
purpureiceps),
EuropeanStarlings(Sturnusvulgaris),American Robins(Turdus
migratorius),and Cedar Waxwings (Bombycillacedrorum).The latter speciesexhibits sucraseactivity, but is
relatively inefficientat digestingsucrose(seeMartinez del Rio et al. 1989).
Species
Fecal sugar•
Dumetellacarolinensis
b
Lamprotornis
purpureiceps
b
Sturnusvulgaris
Turdusmigratorius
14.5 ñ 3.4 (8)
11.6 _+2.9 (4)
11.5 ñ 2.1 (7)
11.6 _+1.1 (4)
This report
This report
Brugger et al. (1992)
Brugger and Nelms (1991)
Reference
Bombycilla
cedrorum
12.1 _+2.6 (10)
Martinez del Rio et al. (1989)
% Brix +- SD (n).
Measurements on day 3 (see text).
this hypothesis is that sucrose-intolerantbirds
should suffer from net water losswhen feeding
on concentrated
sucrose solutions.
Indeed,
imal possible contribution of maltose to the
energy intake of D. carolinensis.
In our calculation we assumedthat luminal digestion of carbohydratesinto oligosaccharidesby pancreatic
amylaseswas not limiting. If maltose concentration is at saturating concentrationin the gut
(Kinfor intestinal maltose hydrolysis in D. car-
American Robins(Turdusmigratorius)
fed on sucrose dramatically increased water consumption (Bruggerand Nelms 1991).In addition, fecal sugarconcentrationin sucrose-fedEuropean
Starlings(Sturnusvulgaris)is approximatelythe olinensisis about 3 mM; Martinez del Rio unindividuals can
sameirrespectiveof the sucroseconcentration publ. data) then D. carolinensis
hydrolyze 0.6 + 0.1 g maltose/h, which proin food (ca. 11% BRIX; Brugger et al. 1993).
Plasmaglucosetestsalso supported the hy- vides 9.6 + 1.6 kJ/h (assuming16 kJ/g of malpothesisthat D. carolinensis
and L. purpureiceps tose;Weastand Selby 1967).The predictedfield
are sucroseintolerant. Although fasting PGL metabolic rate of a D. carolinensis individual
was variable, the negative correlation between weighing 36.3 g is 131 kJ/day (Nagy 1987).Durfasting PGL and the increase in PGL after a ing a 12-h day, catbirdscan hydrolyze a maxiglucose:fructosechallenge indicates that in D. mum of about 115 kJ maltose/day, or 88% of
their metabolic
needs. Dumetella carolinensis incarolinensis
a maximal PGL of about 536 mg/100
ml is defended (Fig. 2). We have no adequate dividuals apparently cannot meet their enerexplanationfor why PGL showed a significant getic demands from maltose alone. Their cadecreaserelative to fasting levels after a sucrose pacity to hydrolyze maltoseis less than that
required to fuel metabolism.Measurementson
challenge.
In vitro measurements
indicated that sucrose
other vertebrate speciesthat possessintestinal
intolerance
in D. carolinensis seems to be caused
sucraseactivity indicatemaltasehydrolytic abilby lack of intestinal sucraseactivity. The mag- ities that are several times higher than those
needed to fuel metabolism on a maltose (or
nitude of intestinal sucraseactivity detectedin
D. carolinensis
in vitrowas too low to be of phys- starch) diet (Hernfindez and Martinez del Rio
iological significance and similar to that re- 1992).
Our resultsalso provide supportfor the hyportedby Martinez del Rio (1990) for two species of thrushes (Muscicapidae). Intestinal
pothesisthat sucroseintoleranceis a shared-demaltase and isomaltasewere present, albeit at rived characterof the sturnid-muscicapid
lineage
low levels. Mean maltase activity in D. caroli- (Martinez del Rio 1990). Although the reasons
nensiswas within the limits predicted for a bird
why sucrase
activitywaslostand why sucrase
has
lacking sucraseactivity, supporting the hy- not been regained in the ancestorof starlings
pothesisthat birds unable to digestsucrosealso and thrushes are unclear, the consequencesof
have reducedmaltosehydrolyzing abilities.The sucraseabsencein this lineage seem to be imavailable data on isomaltaseactivity in birds is portant. Lack of sucraseactivity seemsto limit
still too scanty to allow comparative conclu- the dietary choicesof a large number of species
sions.
(Martinez del Rio and Stevens 1989) and also
To evaluatethe possibleconsequences
of reduced maltose hydrolysis for birds lacking intestinal sucraseactivity, we calculatedthe max-
probably plays a significant role in the interactionof birds with the plantswhose seedsthey
disperse.Sucroseintolerancein starlings,mim-
176
MALCARNEY,
MARTINEZ
DELRIO,ANDAPANIUS
idsand thrushesappearsto be a strongselective
force that contributes
to the maintenance
of low
sucroseconcentrationsin fruit pulp and to the
prevalenceof glucoseand fructosein presentday bird-dispersedplants (Martinez del Rio et
al. 1992).Sucroseintolerancein birds may be a
good example of the implicationsthat single
and seeminglytrivial evolutionaryevents,such
asthe lossof activity in a single multifunctional
enzyme, can have on the interaction between
animals and plants.
[Auk,Vol. 111
lution in the starlings.Bull. ChicagoAcad. Sci.
11:269-298.
BENT, A. C.
1948.
Life histories of north American
nuthatches, wrens, thrashers, and their allies. Bull.
U.S.
Natl.
Mus.
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ACKNOWLEDGMENTS
This manuscript is the result of a collective effort.
We are grateful to those that participated in its com-
pletion. H. Suthersand E. Stileshelped in the capture
of catbirdsand in conditioning them for releaseafter
experiments.Catbirds were captured under permit
PRT-761796(U.S. Fish and Wildlife Service).C. Sheppard and A. Lyles generouslyprovided the Purpleheaded Glossy-Starlings and commented on the
manuscript.L. Eguiarte,K. Brugger,D. Levey,A. Masters, and D. O'Brien read and criticized
drafts of the
manuscript.D. W. White, K. G. Murray, and G. D.
Schnellconstructivelyreviewed the manuscript.Our
work was funded by an NSF grant to C.M.R. (BSR-
BRUGGER,
K. E., P. NOL, AND C. I. PHILLIPS. 1993. Re-
pellency of sucroseto EuropeanStarlings:Will
high-sucrose
cultivarsdeterbird damagein fruit
crops?Ecol. App1. 3:256-261.
COHEN,g. g. 1966. Anticoagulation,centrifugation
time and sample replicate number in the microhematocrit
method
for avian
blood.
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