Download effects of fat stores, migration distance, and diet

The Auk 118(3):665-677, 2001
COMPARATIVE
FUEL
USE OF MIGRATING
FAT STORES, MIGRATION
LEONARD
PASSERINES:
EFFECTS
OF
DISTANCE, AND DIET
Z. GANNES t
Departmentof Ecologyand EvolutionaryBiology,PrincetonUniversity,Princeton,New Jersey08544, USA; and
Mitrani Department
of DesertEcology,
Blaustein
Institutefor DesertResearch,
Ben-GurionUniversityof theNegev,
Midreshet Ben-Gurion, 84990, Israel
ABSTRACT.--Lipids
are the dominant fuel sourceduring migratory flight, but the factors
controllingthe relative importanceof lipid, protein, and carbohydrateto flight metabolism
remain unclear.I tested the nonexclusivehypothesesthat diet, migrationdistance,or endogenouslipid reserves mediatevariation in the fuels birds catabolizeduring migration.
Bloodplasmametaboliteconcentrations
were significantlydifferent amongspecies,and indicated clear differencesin protein and lipid utilization among three turdid chat and five
sylviid warbler speciescaughtduring spring migrationin the Negev Desert, Israel. Fruiteating species(omnivores)catabolizedless protein and morelipid during migrationthan
insectivores.Metaboliteconcentrations
of omnivorousBlackcaps(Sylviaatricapilla),Garden
Warblers (S. borin), and Lesser Whitethroats (S. curruca) were consistent with low rates of
proteolysis(low uric acid), and high ratesof lipolysis (high free-fatty acid and •3-hydroxybutyrate). On the other hand, metaboliteconcentrationsof insectivorousRedstarts(Phoenicurusphoenicurus),
Nightingales (Lusciniamegarhynchos),
Thrush Nightingales(L. luscinia),
Barred Warblers(S. nisoria),and Orphean Warblers(S. hortensis)indicated increasedproteolysisand decreasedlipolysis.Blood metaboliteconcentrations,however,were not correlated with migrationdistance,and the resultsdo not support the hypothesisthat long-distance migrants use fuel differently than short-distance migrants. Triacylglycerol
mobilization was positively correlated with the amount of visible subcutaneousfat, but
blood metabolitecompositionwas more stronglyaffectedby diet. Omnivoresand insectivoresexhibit different fuel-usestrategiesto overcomethe physiologicalchallengesof migration.Received
29 March 2000, accepted
28 February2001.
LIPIDSAREan energy-densefuel source for
volant migrants, and provide the majority of
the energy used during long-durationflights
in birds (Rothe et al. 1987, Ramenofsky1990,
off, burst flight, and fuel delivery to glucosedependent tissues (e.g. central nervous system; Rothe et al. 1987, Schwilch et al. 1996,
Jenniand Jenni-Eiermann1998). Unlike lipid
Jenni-Eiermann and Jenni 1991). Previous au- and carbohydratereserves,protein is stored
thors have suggestedthat only lipids are ca- as functioning tissues.The roles of oxidized
tabolized, and that protein massremains con- protein during migration are likely multifacstant during migration (e.g. Odum et al. 1964). eted and may includereplacingKrebscycleinHowever, body-masschangespreceding and termediaries,maintaining water balance,supduring migration (Marsh 1983, 1984; Piersma plying amino acids for gluconeogenesis,or
and Jukema1990, Wingfield et al. 1990, Lind- balancing changesin mass-dependentpower
str6m and Piersma 1993, Karasov and Pinrequirements (Biebach 1996). However, the
show 1998, Klassen et al. 2000) and direct
mechanisms controlling fuel composition
evidence from blood metabolites (Jenni-Eier(contribution of lipid, protein, and carbohymann and Jenni 1991, Bairlein and Totzke
drate) during migration remain enigmatic.
1992)indicatethat carbohydratesand proteins
Previous studies are compatible with the
also are oxidized during migration. Carbononexclusivehypothesesthat migration dishydrate storesare small relative to lipids, but
tance or endogenouslipid reserves,or both,
glycogenplays an important role during take- mediate variation in the fuels birds catabolize
• Present address: Environmental Studies, Prescott
College,220 Grove Avenue,Prescott,Arizona 86301,
USA. E-mail: [email protected]
665
during migration.A long-distancemigrant,the
GardenWarbler(Sylviaborin),usedlessprotein
and more lipid during fall migration than a
short-distancemigrant, the European Robin
666
LEONARD
Z. GANNES
[Auk, Vol. 118
Distribution
(Erithacus rubecula;Jenni-Eiermann and Jenni
1991). Alternatively, the quantity of endogenous lipid reservescould explain the observed
fuel-use differences.In the abovestudy, European Robins had smaller visible fat reserves
than Garden Warblers (Jenni-Eiermann and
Jenni 1991). Lean passerines,captured in the
Sahara during fall migration, had elevated
Lus.'iniamegarh
Nightingale
Turd Luscinia
luscinia
• •
Thrushnightingale
blood concentrations of urea, consistent with
Phoenicuruspho
increasedprotein oxidation,comparedwith fat
birds (Bairlein and Totzke 1992). A controlled
study of birds varying in both migration distance and fat reservesis required to disentangle thesealternativeexplanationsfor fuel-use
differencesamongspecies.
An alternative factor that has not previously
been explored in migrating birds is that diet
during and precedingmigration might affect
the compositionof fuel oxidized during migration. Daysto weeksof eatinga diet type changes both substrateutilization and storagerates
in exercisinghumansand rats(reviewedin Volek 1997, Hawley et al. 1998, Spriet and Peters
1998). Similarly, the daily nitrogen requirementsof strictly frugivorousand nectarivorous
birds
are lower
than
omnivores
Diet
Redstart
Sylvia
nisoria
Barred warbler
Sylvia
hortensis
Orpheanwarbler
Sylvia
curruca
Lesser whitethroat
Sylviidae
Garden
warbler •.-•'I•
or carnivores
(reviewed in Bairlein and Gwinner 1994; Mur-
Sylvia
atricapilla
Blackcap
phy 1996). Although the effect of diet on the
fuel compositionof migrating birds is completely unknown, diet affectsthe rate of mass
F•G. 1. Closely related sylviid and turdid species
gain during migratory stopover(Bairlein and migrate both short and long distances,and eat both
Gwinner 1994, Parrish 1997).
insectivorous
and fruit-based
omnivorous
diets. The
In the present study, I used a comparative cladogramwas adapted from phylogeniesby Sibley
approachto test the nonexclusivehypotheses and Ahlquist (1995) and Blondelet al. (1996). Distrithat migrationdistance,fat reserves,or diet ex- bution maps indicate northern and southern explain the differencesin fuel use during migra- tremesof winter and breeding ranges(from Cramp
1988, 1992). Specieswere categorizedas mostly intion. Old World warblers (Sylviidae)and chats
sectivorous(fly) or omnivorous(berry) accordingto
(Turdidae) are an excellentrepresentativesys- Cramp (1988, 1992), and dietary assignmentsagree
tem to test these hypotheses.Closely related
sylviid and turdid speciesmigrate both short
and long distancesand eat omnivorousand insectivorousdiets (Fig. 1). If migrationdistance
were an important determinant of migratory
fuel use, then a species' migration distance
shouldbe positively correlatedwith lipid oxidation and negatively correlatedwith protein
oxidationduring migratory flight. Alternatively, if the fuels catabolized during migration
were mediated by endogenouslipid reserves,
then lean birds should have increased
levels of
proteolysisand decreasedlevels of lipolysis
comparedwith fat birds. Finally, if diet mediates the fuels oxidized during migration, fuel
with observations in the field (see methods).
compositionshould group according to diet
type rather than lipid reservesor migration
distance.
METHODS
This study focused on three turdid chats:Redstarts (Phoenicurusphoenicurus),
Nightingales (Lusciniamegarhynchos),
and Thrush-Nightingales(L. luscinia); and five sylviid warblers: Blackcaps(Sylvia
atricapilla),Garden Warblers,LesserWhitethroats(S.
curruca),Orphean Warblers(S.hortensis),
and Barred
Warblers(S. nisoria).Birdswere captured in mist nets
July2001]
FuelUsein Passerine
Migrants
in the gardens at Midreshet Ben-Gurion, Israel
(30ø52'N, 34ø46'E, 476 m above sea level). Located in
the northern Negev Desert, Midreshet Ben-Gurion
receives<100 mm rainfall annually.
Migrants were capturedin mist nets daily 4 March
to 18 May 1996 and 10 March to 21 May 1997. The
nets were
checked
at 15-20
min
intervals
from
1 h
667
In this study,I used free-fatty acidsand •3-hydroxybutyrate concentrationsas indicatorsof lipid turnover, and uric acid as an indicator of protein turnover. However, I do not assume that glycerol,
triacylglycerol, or glucoseconcentrationswere correlated
with
turnover.
Radar data from the Negev Desert indicated that
beforesunriseand for approximately4 h thereafter. migrating passerinesland at dawn (Bruderer and
High midday temperaturesand frequent afternoon Liechti 1995). Becausethe goal of this study was to
windstormsprecluded capturing birds all day long. comparefuel use during flight, new-arrival and reFlattenedwing cord and mass(Ohauselectronicbal- capturebirds were sampledonly during the first 2 h
ance +0.1 g) were measured,and birds were banded after twilight. Twilight times were calculatedusing
with
aluminum
bands obtained
from
the Israel
the program availablefrom the Australian DepartBanding Center.In addition, visual subcutaneousfat ment of Industry, Scienceand Tourism. Time after
was scored in half-units
from 0 for no visible fat to 4
twilight was included asa factorin statisticalmodels
for lipid storageregionsoverflowingwith fat (mod- (see below).
ified from HelmsandDrury 1960).Fatscoreexplains
To obtainblood samples,I puncturedthe vena ul-50% of the variation in total body fat of other mi- naris with a 26 gauge hypodermic needle and colgrant passerines(Rogers 1987, Krementz and Pen- lectedthe blood in heparinizedcapillary tubes(60dleton 1990,Sprengleret al. 1995),particularlywhen 120 [tL). Blood samples were kept on ice for a
interobserver variation is reduced (Krementz and
maximum of 3 h until they were spun in a microhePendleton1990).Throughoutboth seasons,threeob- matocrit centrifuge (5 min, 12,000 g). Blood metabservers were frequently crosscheckedfor internal olite concentrations
did not changesignificantlyover
consistency
in scoringfat. Birdswere generallyheld this time period (L. Gannes unpubl. data). I mea<30 min, including time spent in the net and sured hematocrit and discarded the red blood cells.
processing.
Blood plasma was diluted gravimetricallyby oneBecausethe samesite was intensivelytrapped dai- half with isotonic saline solution, and diluted samly, individuals captured without a band (after the pleswere storedat -80øC until analyzed.
first 10 days)were callednewarrivals.Birdscaptured
Triacylglycerol,glycerol,uric acid, •3-hydroxybu->1 day after their first capture were termed tyrate, glucose(SigmaDiagnostic,St. Louis,Missourecaptures.
ri) and free-fatty acid (Boehringer-Mannheim,IndiBloodmetabolite
analyses.--Evidence
for lipid, pro- anapolis, Indiana) concentrationswere analyzed
tein, and carbohydrate catabolism can be found in using spectrophotometric
assaysmodified for small
the blood,becausethe majority of an animal'senergy volumes.The triacylglycerolvaluesreported in this
reservesare stored externally to metabolizing cells. study were calculatedby subtractingfree glycerol
Lipolysis is associatedwith elevatedconcentrations from the total bound and unbound glycerol ("true
of free-fatty acid, glycerol,and [3-hydroxybutyrate, triacylglycerol").Absorbancevaluesof samples(in
and elevated triacylglycerol levels are associated duplicate, 3-10 [tL) and standards were measured
with net lipogenesisin the liver (Hurley et al. 1986, with a spectrophotometer.
Jenni-Eiermannand Jenni1992,1994).Bloodplasma
Migration distance.--Minimumand maximum mifree-fatty acid concentrations
were significantlycor- gration distanceswere compared among species.
related (r = 0.9446, Pearson correlation P = 0.0045) The minimum migration length was calculatedby
with lipid turnover in chickens(Gallusgallusdomes- subtracting the northernmost wintering from the
ticus)run on a treadmill (reanalysisof data from Vin- southernmostbreeding ranges, in degreeslatitude
cent and Brackenbury1988). In addition, free-fatty (Cramp 1988, 1992).Similarly,the maximum migraacid and [3-hydroxybutyrateconcentrationswere tion distance was calculated by subtracting the
positively correlatedin flying and resting pigeons southernmost wintering from the northernmost
(mean r = 0.783 _+0.042; Gannes et al. 2001). Uric
breeding ranges. Becausethe two measuresof miacid is the major end product of protein catabolism gration distancewere significantlycorrelated(pairin birds. In a variety of birds,bloodplasmauric acid wise correlation,R; 0.884,P = 0.0036),only the reconcentrationswere correlated with protein oxida- sults from the minimum migration distance were
tion measured by excreted nitrogen (Mori and reported below.
George 1978, Robin et al. 1987, Cherel et al. 1988,
Diet.--I usedCramp (1988,1992)for assigningdiet
Lindggrd et al. 1992).In contrast,blood glucosecon- types to species.During the nonbreeding season,
centrationsare not necessarilycorrelated with glu- Blackcaps, Garden Warblers, and Lesser Whitecoseoxidation. Many birds regulate blood glucose throats depend to a large degree on noninsectfood
concentrationswithin narrow limits (e.g.Hazelwood sources (berries and fruits), and will be referred to
1986, Swain 1992a),but somespeciesapparently do as omnivores.On the other hand, Nightingales,
not (e.g. Swain 1987,Jenni-Eiermannand Jenni1997). Thrush-Nightingales, Redstarts, Barred Warblers,
668
LEONARDZ. GANNES
[Auk, Vol. 118
TABLE1. Resultsfrom separateANCOVA modelsfor glycerol,triacylglycerol,free-fattyacid,uric acid, •hydroxybutyrate,and glucoseconcentrationin new-arrival passerinemigrants.Fat (visiblesubcutaneous
fat score)and Timeof day(hoursafter twilight) were includedas covariatesand Species
and Yearwere includedas factors.Significanteffectsare in bold.
Fat
Metabolite
Slopea
Glycerol
Triacylglycerol
Free-fattyacid
0.046
0.240
-0.014
Uric acid
-0.036
•-hydroxybutyrate
Glucose
PC1
PC2
0.027
0.145
-0.058
0.195
F
Species
P
F
2.2 0.1432
13.9 0.0003
0.0 0.8920
1.3
2.8
2.7
0.8
0.3613
5.0
0.1
0.7425
4.0
0.3
0.6
5.1
0.5873
0.4491
0.0263
4.7
10.3
2.4
Year
P
F
0.2418
0.0095
0.0121
<0.0001
0.0004
0.0001
<0.0001
0.0249
Time of day
P
F
n
2.0
0.2
2.7
0.1599
0.6240
0.1000
2.1
0.1498
3.4
0.0684
180
0.7
0.4199
4.1
0.0437
159
3.9
6.0
0.0
0.0514
0.0159
0.9996
131
122
122
49.0
2.0
10.0
<0.0001
0.1646
0.0020
2.3
0.0
0.0
P
0.1305 180
0.8916 180
0.9236 171
Slopeof ANCOVA effectof fat on metaboliteconcentrations,
significantslopesare in bold.
and Orphean Warblers take almost exclusivelyinsects,and will be referred to asinsectivores.
Although
many avian migrantschangedietsduring migration
(reviewed in Bairlein and Gwinner 1994), observations from Midreshet Ben-Gurion agreed with
Cramp'sdietary generalizations.Approximately2030% of the Blackcaps,Garden Warblers,and Lesser
Whitethroats captured in 1997 had plant parts in
their feces, or their bill, forehead, and crown were
coveredwith pollen and nectar (L. Gannesunpubl.
data). The defecatedseedswere mostly from acacia
pods (Acaciasp.)and the acaciatreeswere oftencovered with feeding Blackcapsand Lesser Whitethroats.In addition,I frequentlysawLesserWhitethroatsprobingflowers,presumablyfor nectar.Less
than 3% of the Redstarts,Orphean Warblers,Barred
Warblers, Nightingales, and Thrush-Nightingales
had plant parts in their fecesand nonewere covered
with pollen (L. Gannes unpubl. data). In addition,
Redstartsand OrpheanWarblersfed adlibitumin the
laboratoryrefusedto eat a fruit-baseddiet ("banana
mash"; Denslow et al. 1987), but readily consumed
mealworms (Tenebriolarvae; L. Gannes unpubl.
data). On the other hand, Blackcapsreadily ate and
gained masson either the fruit-basedor mealworm
diets (L. Gannesunpubl. data).
Statisticalanalyses.--Separate
ANCOVA modelsfor
eachmetabolitewere used to interpret interspecific
and recapturedbirds, and betweenomnivoresand
insectivores.
Both models
included
time after twi-
light as a covariate,and year and speciesas factors.
Principal componentanalysis(PCA) was used to
clarify interspecificvariation in blood-metabolite
concentrations.
PCA
combines
correlated
variables
into independentand interpretableaxes.The new
PCA values can then be used to comparecorrelated
variables among species.All six blood metabolites
were usedin the PCA,but birds missingoneor more
metabolite
measures
were
excluded
from
the
analysis.
The data in the ANCOVA
models did not meet the
assumptionsof normality. Natural-log transformed
variablesdid meetthe assumptionsof normality,but
the transformationsdid not changethe resultsqualitatively. Therefore,data were not transformedbefore analysis.Discrepanciesin samplesize are a result of incompletesamples,and all meansare given
_+SE.Statisticalmodelsand PCA were analyzed using JMP 3.1 for the Macintosh(SASInstitute 1994).
RESULTS
Interspecific
bloodmetabolites.--Blood-metabolite concentrationsof newly arrived birds
were significantlydifferent amongthe species
differences in blood metabolites, with fat score as a
independentof fat score(Table1). In newly arcovariate.We included time after twilight as a cov- rived birds, free-fattyacid valueswere highest
ariate in all ANCOVA models, because previous in Blackcaps
and GardenWarblers,and lowest
studies have found that metabolite
concentrations
in Redstarts,Nightingales,and OrpheanWarchangeover the courseof the day (Jenni-Eiermann blers(Fig. 2). Blackcaps,
GardenWarblers,and
and Jenni 1997, Jenni and Jenni-Eiermann 1996). Year
Lesser
Whitethroats
had
significantly lower
was also included to control for differences between
1996 and 1997.The least squaremeans(LSM) from
the ANCOVA
models were used to make ad hoc com-
parisons of metabolite values independent of fat
score,time after twilight, and year. Similarly, ANCOVA models were used to interpret blood-metabolite
concentration
differences
between
new-arrival
uric acid concentrations
than redstarts
or Or-
phean Warblers (Fig. 2). Blackcaps,Garden
Warblers,and LesserWhitethroatshad higher
plasma •3-hydroxybutyrate
levelsthan Nightingales, Redstarts,and Thrush-Nightingales
(Fig. 2). Glycerol concentrationswere not sig-
July2001]
3.0
FuelUsein Passerine
Migrants
ab
a
a
b
b
ab
a
ab
669
1.0-
il; t 0.8
20
23
54
34
8
0,2
6
8
26
55
34
21
ac
ad
a
b
bc
cd
a
3.0
ac
e•
;i[i
8
20
25
58
20
9
ac
a
ab
b
a
b
8
21
26
55
34
21
6
0.0--
a
a
bc
bc
c
ab
ac
ab
ab
9
6
P '-- 0.0095
0.0
a
6
1.0
P < 0.0001
34
9
P = 0.1432
0.0
.•1
3.0
21
P = 0.0121
0.0
1.5-
18
30.0
ac
ac
b
c
bc
ac
bc
6
11
18
48
25
9
8
a
2.0
•'• 20.0
1.0
8
0.0
15
22
56
29
14
9
6
P= 0.0004
........
L1
Lm Pp Sa Sb Sc Sh Sn
15.0
5
P= 0.0001
L•ILm
' Pp
' S•tS• S• S[•Sn
'
FIG.2. Blood-plasma
concentrations
(retool/L)of free-fatty
acids,uricacid,•-hydroxybutyrate,
glycerol,
triacylglycerol,
and glucosesignificantly
vary amongmigratoryspecies.
Least-square
means(LSM ___
SE)
givenfor furdidchats(squares):
Thrush-Nightingales
(L1),Nightingales
(Lm),Redstarts
(Pp);andsylviid
warblers(circles):
Blackcaps
(Sa),GardenWarblers(Sb),LesserWhitethroats
(Sc),OrpheanWarblers(Sh),
BarredWarblers(Sn).P-valuesindicateresultsof speciesdifferencesin ANCOVAmodels(Table1), and differentlettersindicatesignificantly
differentmeans,by linearcontrasts.
Samplesizesgivenbelowtheerror
bars.Omnivores
andinsectivores
areindicated
by filledandemptysymbols,
respectively.
nificantlydifferentamongthe species(Fig. 2).
explained48% of the variation (Table2). The
Plasma triacylglycerolconcentrationsin new- first principalcomponentaxis(PC1)wasposiarrival Blackcapsand Lesser Whitethroats tively correlated with concentrationsof free-
were lower than those of Garden Warblers,
fatty acidsand •-hydroxybutyrateand negaNightingales,and Thrush-Nightingales(Fig. tively correlated with concentrationsof uric
2). Redstartsand GardenWarblershad higher acid and triacylglycerol(Table 2). PC1 exlevelsof plasmaglucosethan BarredWarblers, plained 26% of the total variance.BecausePC1
Nightingales,or Thrush-Nightingales
(Fig.2). was positively correlatedwith lipid metaboPrincipalcomponentanalysis(PCA)clarified lites and negativelycorrelatedwith uric acid,I
the complexpatternsof interspecific
bloodme- interpretedPC1 as the "lipolysis-proteolysis
tabolites.The first two principalcomponents axis."PC1valuesfromBlackcaps,
GardenWar-
670
LEONARD
Z. GANNES
[Auk,Vol. 118
TABLE 2.
Results from PCA of blood metabolites for
TABLE3. Least square means (LSM + SE), minimum
and maximum
visible
subcutaneous
fat
new-arrival migrants. Valuesindicate correlation
coefficientsof first (PC1) and second principal
scoresfor studyspecies.LSM from ANOVAmodel
componentaxes(PC2). PC1 was positivelycorreof species(F = 5.92, df = 7 and 183,P < 0.0001)
lated with lipid metabolites(B-hydroxybutyrate, controllingfor year (F = 25.9, df = 1 and 183,P <
free fatty acids),negativelycorrelatedwith protein
0.0001).Differentlettersindicatesignificantlydifmetabolite(uric acid), and interpreted as the "liferentmeansby linear constrasts.
polysis-proteolysis
axis."PC2waspositivelycorrelatedwith lipid metabolites(glycerol,triacylgly- Species
Fat score Min Max n
cerol, free-fatty acid), negatively correlatedwith
2.19 + 0.3b 0.5 3.5 8
glucoseconcentration,and interpretedas the "li- ThrushNightingale
(Luscinialuscinia)
polysis-glycolysis
axis."
Nightingale
1.96 +_0.19b 0.5 3.0 21
(L. megarhynchos)
Metabolite
PC1
PC2
% Explained
Glycerol
Triacylglycerol
Free-fattyacid
26
0.12
- 0.42
0.45
Uric acid
-0.75
•-hydroxybutyrate
22
0.52
0.64
0.50
0.72
Glucose
-0.03
Redstart
0.81 _+ 0.17 a
(P.phoenicurus)
Blackcap
(Sylviaatricapilla)
1.68 _+0.11b 0
4.0 58
Garden
1.25 _+ 0.15 a
0
2.5
34
1.81 _+ 0.19 b
0
3.5
21
Warbler
0.13
(S. borin)
0.22
Lesser Whitethroat
-0.65
0
2.5
26
(S. curruca)
Orphean Warbler
(S. hortensis)
2.24 _+0.30b 0
3.0
9
Barred Warbler
2.21 _+ 0.37 b
3.0
6
2.0
(S. nisoria)
biers, and LesserWhitethroatsindicatedhigh
levelsof lipolysisand low levelsof proteolysis,
but metabolitesfrom Orphean Warblers,Redstarts, Nightingales, Barred Warblers, and
Thrush-Nightingalesindicatedlow levelsof lipolysisand high levelsof proteolysis(Fig. 3).
The second principal component axis (PC2)
wasnegativelycorrelatedwith glucoseconcentration and positivelycorrelatedwith glycerol,
triacylglycerol,and free-fatty acid concentrations.This axis explainedan additional22% of
LLm•
SnlSa
r•
b-•b
•Sc
- 0.5
1.5
i
i
-0.5
0
UA, TAG
PC1
Proteolysis
i
0.5
i
1
FF^, •-HB^
Lipolysis
F•G.3. Protein and lipid oxidationduring migration significantly differ among species.The first
(PC1) and second(PC2) principalcomponents
were
interpreted as the "lipolysis-proteolysis"and the
"lipolysis-glycolysis"axes,respectively(SeeTable
2). PC1valuesfrom Blackcaps,
GardenWarblers,and
LesserWhitethroatsindicatedhigh levelsof lipolysis
and low levelsof proteolysis,but metabolitesfrom
OrpheanWarblers,Redstarts,Nightingales,Barred
Warblers, and Thrush-Nightingalesindicated low
levelsof lipolysisand high levelsof proteolysis.Redstartsand OrpheanWarblershad significantlylower
PC2 valuesthan Nightingales,Thrush-Nightingales,
Blackcaps,and Barred Warblers.Valuesare LSM _+
SE.SeeFigure2 for explanationof symbolsandTable
i for full ANCOVA
models.
the overall variance (Table 2). PC2 can be inter-
preted as the lipolysis-glycolysisaxis. Redstartsand OrpheanWarblershad significantly
lower PC2 valuesthan Nightingales,ThrushNightingales, Blackcaps,and Barred Warblers
(Fig. 3).
Fat stores.--Althoughthere was a large variation in fat score,only triacylglycerolconcentrations were significantlycorrelatedwith fat
score.Among species,birds coveredthe entire
fat-scorerange(0-4), and mostspeciesalsohad
individuals from all categories(Table3). Garden Warblersand Redstartshad significantly
lower fat scoresthan any of the other species
(Table3). ANCOVA analysesindicatedthat fat
scorecovariedwith triacylglycerolvaluesregardlessof speciesdifferencesand controlling
for year and time after twilight (Table1). Not
surprisingly,PC2 was also positively correlat-
July2001]
FuelUsein Passerine
Migrants
671
Sa
•.•
0.5
0
Sh
• tSn
•
S -1.0
R = 0.168, P > 0.6
i
i
10
15
i
20
i
25
i
30
i
35
40
v
v
Minimum migrationdistance(degreeslatitude)
FIG. 4. Minimum migration distance did not explain the variation of lipid and protein use in migrating songbirds.Least-squaremeans(LSM _+SE)
of the first principalcomponent(PC1) were not significantly correlatedwith a species'minimum migration distance(R and P for pairwise correlations).
Migration distancetaken from Cramp (1988, 1992).
SeeFigure 2 for explanationof symbolsand Table1
for completeANCOVA model.
v
ed with fat score, because PC2 is associated
with triacylglycerolconcentrations(Table 2).
However,the covarianceof fat scorewith glycerol, glucose,free-fatty acids,uric acid, fi-hydroxybutyrate and PC1 were not significant
(Table 1).
Migrationdistance.--Thewintering rangesof
the sylviids and turdids in this study span
from north of the equatorto the southerntip of
Africa, and the breeding rangesbegin in the
northern
Mediterranean
and
most
extend
above the Arctic Circle (Fig. 1; Cramp 1988,
1992). The species'meansof the first principal
componentaxis (PC1) were not correlatedwith
minimum migrationdistanceof a species(pairwise correlations;
Fig. 4). Similarly,noneof the
individual metabolitesor PC2 correlatedsignificantlywith minimum migrationdistance(P
> 0.2).
Diet.--Diet explained much of the variation
in bloodmetaboliteconcentrations
of newly arrived migrants (Table 4). Fruit-eating omnivores(Blackcaps,Garden Warblers,and Lesser
Whitethroats)had significantlyhigherfree-fatty acid and fi-hydroxybutyrate,and lower uric
acid and triacylglycerolplasma concentrations
than insectivores (Orphean Warblers, Redstarts, Barred Warblers, Nightingales, and
+1 +1 +1 +1 +1 +1 +1 +1
c.l I
I
672
LEONARD
Z. GANNES
[Auk, Vol. 118
Thrush-Nightingales). As a result, omnivores
had significantly higher means on the lipolysis-proteolysisaxis (PC1) than did insectivores
(Fig. 2). Glycerol, glucose,and PC2 were not
significantlydifferentbetweenthe diet groups
(Table 4).
Metabolitesof newly arrived and recaptured
birds.--A five-speciessubset (Lesser Whitethroat, Nightingale, Redstart, Blackcap,Garden Warbler) of the eight study specieswere recapturedin large enoughnumbersto compare
blood metabolite concentrationsof newly arrived and recaptured birds. Repeated measures on the same bird were not possible,because few birds were sampled both as new
arrivals and recaptures.Newly arrived birds
had significantlyhigher glyceroland free-fatty
acid, and lower uric acid concentrations than
recapturedbirds (Table5). Bloodglucose,•3-hydroxybutyrate and triacylglycerollevelswere
not significantlydifferent betweennew arrival
and recaptured birds (Table 5). In addition,
blood hematocritvalueswere significantlylower in recaptured (0.443 ___
0.007) than in new arrival birds (0.492 +__
0.004; F = 46.1, df = i and
190, P < 0.0001), but neither species(F = 1.9,
df = 4 and 190, P > 0.1) nor year (F = 0.2, df
= i and 190, P > 0.6) were statistically
significant.
DISCUSSION
Blood plasma metabolite concentrations
were significantlydifferent amongspeciesand
indicatedclear differencesin protein and lipid
utilization.
Metabolite
concentrations
in Black-
caps, Garden Warblers, and Lesser Whitethroatswere consistentwith low levelsof proteolysis (low uric acid), and a high degree of
lipid oxidation(indicatedby high free-fattyacids and 13-hydroxybutyrate;
Fig. 2). On the other hand, metabolite concentrations of Red-
starts, Nightingales, Thrush-Nightingales,
Barred Warblers, and Orphean Warblers suggesteda higher level of proteolysisand lower
lipolysis (Fig. 2). PCA separatedspeciesalong
the lipolysis-proteolysisaxis (PC1; Fig. 3). The
resultswere consistentwith Blackcaps,Garden
Warblers, and Lesser Whitethroats using less
protein and more lipids during migrationthan
Redstarts,Orphean Warblers,BarredWarblers,
Nightingales,and Thrush-Nightingales.
vvv
July2001]
FuelUsein Passerine
Migrants
Levels of proteolysis and lipolysis clearly
groupedaccordingto diet. Fruit-eatingomnivores(Blackcaps,Garden Warblers,and Lesser
Whitethroats;Fig. 1) had lower uric acid, and
higher free-fatty acid and [•-hydroxybutyrate
concentrations than insectivores (Orphean
Warblers, Redstarts, Barred Warblers, Nightingales, and Thrush-Nightingales;Table 4).
Speciesshare a commonevolutionaryhistory,
and variousauthorshave pointed to the statistical pitfalls of treating speciesas statistically
independentobservations(reviewed in Felsenstein 1985, Garland and Carter 1994). However,
673
Diet potentially can affect fuel use in flight
by long-termbiochemicaladaptationto a diet,
short-term replenishment of endogenousreserves,or both. The daily nitrogen requirements of frugivorous and nectarivorousbirds
are lower than omnivores or carnivores (re-
viewed in Bairlein and Gwinner 1994,Murphy
1996), and changingdiet type for a period of
days to weeks affects substrateutilization in
exercisinghumansand rats (Hawley et al. 1998,
Spriet and Peters 1998). However, proximate
mechanismsof dietary adaptationare not well
understood, and it remains unclear how diet-
induced fuel-use differences might translate
sectivorous Orphean and Barred warblers into fuel-use differences during migratory
closelyresembledthe concentrations
of insec- flight. Alternatively,dietary intake and compositionhasa short-termeffect,takinghoursto
tivorous turdid chats rather than their omnivcarbohydrate
orous congeners(Fig. 1). Migratory fuel-use days,on an animal'sendogenous
stores
(Hazelwood
1986,
Swain
1992a, Spriet
splittingaccordingto dietarypreference,rather
than phylogeneticrelationships,supportsthe and Peters1998). Becauseglycogenstorescan
hypothesisthat diet wasa moreimportantfac- be depletedquicklyduring exerciseand are retor in migratory fuel-use than phylogenetic plenishedindependentof lipid reserves,evena
highly obesemigrant may have very reduced
history.
glycogen reserves after a nocturnal flight.
Some individuals
labeled
as new arrivals
Fruit-eating omnivores eating carbohydratemay not have been captured when they first
rich diets (i.e. fruit, nectar)may havelarger glyarrived at the study site, but severallines of
cogenreservesat the beginningof a migratory
reasoningsuggestthat blood-metaboliteconflight than insectivoreseating carbohydratecentrationsof new-arrival birds were represenpoor diets, similar to mammals (reviewed in
tative of in-flight concentrationsof migrating
Volek 1997, Hawley et al. 1998, Spriet and Pebirds. First, sampleswere only taken during ters1998).In postabsorptive
animalswhen glythe period when radar indicatedmost passer- cogenstoresare reduced, protein becomesthe
ines make landfall (Bruderer and Liechti 1995).
dominant precursor for gluconeogenesis
Second,only a small minority of the individu- (Maughan et al. 1997).As a result, a bird with
als remainedat the sitefor longerthan oneday. large glycogenstoresmay catabolizelessproEightyto 90% of the migrantsin 1996and 1997 tein to maintain blood glucoselevels during
were only captured once,and the majority of migration than a bird with small glycogenrethosebirds probablycontinuedmigrating the serves.In addition,the two effectsprobablyare
sameeveningof the day they arrived (L. Gan- not mutually exclusiveand couldactin concert:
nes unpubl. data). Third, blood metabolites enzymatic activity reducing body tissues'glu(glycerol,free-fatty acid,uric acid) and hemat- cose requirements,and therefore conserving
ocrit were significantlydifferentbetweennew- glycogenreservesand thusbody protein.Howarrival and recaptured birds, suggestingthey ever,without knowing the stopoverand feedcamefrom two different "groups" (Table5). Fi- ing history of individual birds, it is impossible
nally,otherwork hasshownthatbloodconcen- to separatelong-term dietary adaptationfrom
trations of glycerol, free-fatty acid, and uric short-termreplenishmentof glycogenreserves.
acid were not significantly different between
The resultsfrom this studyarenot consistent
EuropeanRobinscapturedin flight and those with the hypothesis that long-distancemicaptured soon after landing (Jenni-Eiermann grantsuse fuel differently than short-distance
and Jenni1991). In the present study, we in- migrants (cf. Jenni-Eiermannand Jenni 1991,
cluded time after twilight as a covariateto con- Jenni and Jenni-Eiermann 1998). Individual
trol for potential changesin metaboliteconcen- blood-metaboliteconcentrationsand principal
component values were not correlated with
tration during the 2 h samplingperiod.
the blood-metabolite
concentrations
of the in-
674
LEONARD
Z. GANNES
minimum migrationdistancesthat varied over
20ølatitude (-2,200 km; Fig. 4). All the species
in the presentstudywinter southof the Sahara,
and crossingthe Saharamay exert similar selectivepressurefor differentialfuel useregardless of total migration distance.However, the
European Robin studied by Jenni-Eiermann
and Jenni(1991) winters on the northern edge
of the Sahara (Cramp 1988), and used more
protein and lesslipid than the Garden Warbler
that winters in southernAfrica (Cramp 1992).
As would be predictedfrom the presentstudy,
the European Robin is mainly insectivorous
[Auk, Vol. 118
and may provideimportantnutrientsand fatty
acids (reviewed in Bairlein and Gwinner 1994,
Parrish 1997). In addition, the present work
suggeststhat the switch from insectivoryto
fruit-eating omnivory is also associatedwith
decreased catabolism of endogenousbody
protein.
We might expect a strong selectivepressure
on insectivores to reduce protein oxidation.
Unlike lipid and carbohydratereserves,protein is stored as functioningtissue.However,
birds may preferentially catabolizeassimilation organsto avoid catabolizingflight musand the Garden Warbler is omnivorous (Bert- cles that could impair flying ability (Swain
hold 1976, Cramp 1988, 1992; L. Gannes un- 1992b,Kaspereket al. 1992, Karasovand Pinshow 1998, Biebach1998). As a result, protein
publ. data).
Previous authors have hypothesized that oxidation may lead to decreasedperformance
speciesdifferencesin fuel use were mediated of absorptiveorgans (e.g. Biebach1998, Karby fat reserves:fat birds usemorelipid and less asov and Pinshow 1998, Piersma 1998), that
protein than thin birds (Jenni-Eiermannand could reduce a migrant's ability to refuel enJenni 1991, Bairlein and Totzke 1992). The re- route. Compared to lipids, protein is a relasuitsfrom thepresentstudypartially agree.Fat tively heavy fuel (Schmidt-Nielsen1990).Probirds had higher triacylglycerolconcentrations tein oxidation actually could reduce the
than lean birds, but none of the other metabo- amount of weight birds must carry during
lites covaried with fat score (Table 1). It seems long-duration flights (e.g. Piersma and Lindthat fat migrantsincreasedtriacylglycerolmo- strom 1997, Piersma and Gill 1998), perhaps
bilization without changingproteolysisor oth- increasingpotential flight range. Ultimately,
er lipolysis metabolites.Migrating passerines the selectivepressureson migrantswill be the
may supply metabolizing cells directly with result of how diet affectstotal migration dutriacylglycerol,circumventing the potentially ration throughproximatefactorssuchasstoprate-limiting albumin-mediatedtransport of over site suitability or availability, stopover
free-fatty acids (Weber 1988, Jenni-Eiermann duration, and maximum migration distance
and Jenni 1992). The present study suggests without refueling. It seems,however,that inthat fat birds might be able to use the triacyl- sectivoresand fruit-eating omnivoresexhibit
glycerolpathway to a greaterdegreethan lean different migrationstrategies,eachwith an asbirds. However,species-level
differencesin fuel sociatedsuite of morphologicaland behavioruseoccurafter controllingfor differencesin fat al adaptationsto overcomethe physicalchallengesof migration.
score (Table 1).
Conclusions.--Spring
migrants minimize the
ACKNOWLEDGMENTS
time spenton migration,presumablyto acquire
good breeding territories (Lindstr0m and A1This researchis dedicated to my grandparents
erstam 1992,Klaassen1996).Over evolutionary (Jackand Molly Rayman, Miriam and Abe Gannes)
time, migrantshave"solved" migrationalchal- who havebeena sourceof inspirationfor as long as
lengeswith a suite of morphologicaland be- I can remember. The fieldwork would have been imhavioral adaptations(reviewedin Bertholdand possible without skilled assistancefrom Wendy
Terrill 1991, Gwinner 1990, Berthold and Hel-
Schelsky,Nathaniel Gerhart, Itai Shani, Nir Sapir,
big 1991, Bairlein 1991). One such adaptation
exhibited by many passerine migrants is
switching from a mainly insectivorousdiet to
a fruit-baseddiet precedingand during migra-
Norm Budnitz, Itamar Giladi, Gilead Michaeli, Kevin
tion (reviewed in Bairlein and Gwinner 1994).
constructive
Schwartz,and Garr. I thank Berry Pinshowfor making facilities availableto me at the Mitrani Department of Desert Ecology,Ben-GurionUniversity,Israel. This manuscript was greatly improved with
comments
on earlier
drafts from Carlos
Switching to a fruit-dominated diet increases Martfnez del Rio, Diane O'Brien, Scott McWilliams,
premigrationaland en-routerate of massgain, Lila Fishman,William Karasov,ChrisGuglielmo,Ulf
July2001]
FuelUsein Passerine
Migrants
Bauchinger,and Herbert Biebach.Insightful commentsfrom two anonymousreviewersimprovedthe
clarity of the manuscript.This work was funded by
a National
Science Foundation
Doctoral
Dissertation
Improvement Grant (# 9623836),a Sigma Xi GrantIn-Aid of Research,and PrincetonUniversityfunds.
The researchwas conductedwith researchpermits
from the Israeli Nature ReservesAuthority. This is
contributionnumber324 of the Mitrani Department
for Desert Ecology.
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