ADAPTATIONS OF THE GRAY DUMETELLA CAROLINENSIS TO LONG DISTANCE MIGRATION: ENERGY STORES AND SUBSTRATE CONCENTRATIONS IN PLASMA

RICHARD L. MARSH • Divisionof BiologicalSciences, The Universityof Michigan,Ann Arbor, Michigan48109 USA

ABSTRACT.--Themajor body components(water, lean dry, and fat) were measuredin the carcassesof Gray Catbirdsfrom which the flight muscleshad been removed. were collectedfrom May throughOctober near Ann Arbor, Michigan and during Septemberand October near Gainesville,Florida. Additionally, the glycogencontent of muscleand liver and the concentrationsof glucoseand triglyceridesin plasmawere determinedin sampledduring fall migrationin Florida. Catbirdsattained maximum body massesof -50 g in Florida,largely due to the addition of fat. Relativelylean birds (-3-4% body fat) in spring throughfall weighedapproximately 35 g. Thirteen percentof the birds sampledwere estimatedto have had sufficientreserves of fat to crossthe Gulf of Mexico, althougha larger proportionof the populationprobably makes this crossing.The lean dry massof the carcass (without the flight muscles)is related significantlyto structuralbody size and time of day, but is not related to molt, sex, or carcassfat content.Plasma glucose and triglyceridesin free-livingfall migrantsdo not vary diurnally. Liver glycogen,however, is four timeshigher in the eveningthan in the morning(77 and 19 mg/g,respectively), and muscleglycogen is five times higher in the evening (20 and 4 mg/g, respectively).Evening concentrationsof glycogenare amongthe highestvalues reported for birds and do not confirmthe reduction in glycogenreported for someother migrants.Received 16 February1982, accepted 30 June 1982.

DuE to the high metabolicdemands of flap- to the extensiveinformation available on lip- ping flight, small birds must anticipatelong- ids, the role of carbohydratebefore and during distance migratory flights by storing large migration is less clear. Although glycogen re- amounts of energy. Energy is stored primarily serves in liver and muscle are depressedand as fat (triglycerides)before migratory flights, diurnal cyclesof glycogencontent damped in and patterns of premigratory fat deposition spring migrants of Ganabel'sWhite-crowned have been describedfor numerousspecies (see Sparrow (Zonotrichialeucophrys gambelii), fall reviews by Farner et al. 1968, King 1972, Bert- migrants of the same specieshave high gly- hold 1975).Small migrants show great cogenlevels (Farner et al. 1961, King et al. 1963). interspecificvariability in suchdeposition. This On the other hand, three spring migrants in variability appearsto be relatedto the distance India, which alsoaccumulate large fat deposits, traveled and the duration of migration (Odum have elevated levels of glycogen(Naik 1963, et al. 1961, Johnston1966, Helms and Smythe Vallyathan and George 1964, John and George 1969), with the greatest reservesbeing accu- 1965) and substantialdiurnal glycogencycles mulated by birds that must make long, non- (George and Chandra-Bose1967) in the pre- stop flights acrossmajor geographicalbarriers migratory period. (Odum et al. 1961, Fry et al. 1970). The major In addition to variations in energy substrates lipid componentsof muscle,liver, and plasma with season and migratory state, various au- also increasein parallel with depot fat content thors have examined the possibility of fluctua- (Farner et al. 1961, King et al. 1963, John and tions in the lean dry mass or the protein con- George1965, de Graw et al. 1979).In contrast tent of migrants. The results obtained from these studies seem contradictory. Odum and i Presentaddress: Department of Biology, North- severalcolleagues (Connell et al. 1960, Odum eastern University, Boston, Massachusetts 02115 et al. 1964, Rogersand Odum 1964)have pro- USA. posed that the lean mass remains approxi- 170 The Auk 100: 170-179. January1983 January1983] Gray CatbirdBody Composition 171

mately constantduring fattening, with only fat METHODS being added, whereas several more recent Capture and initial observations.--Catbirds were studies have documented an increase in the mist-netted near Ann Arbor, Washtenaw County, lean dry componentof the body massas birds Michigan and Gainesville, Alachua County, Florida. fattenfor migration(Evans 1969, Fry et al. 1970). Birds were capturedin Ann Arbor during fall, 1975, Theseincreases have been thoughtto represent and spring through early fall, 1977.Florida captures an addition of protein, to form a protein "re- took place in the falls of 1976 and 1977. Except as serve"of use during migration (Fry et al. 1972, noted below, the birds were returned to the labora- Ward and Jones 1977). tory alive, and the following data were recorded on In associationwith studiesof adaptationsof the live birds within 2 h of capture: body mass to the flight musclesof the Gray Catbird (Dume- the nearest 0.1 g, visual fat class (1-5; based on a tella carolinensis)to long-distance migration scheme similar to that of Morton et al. 1973), wing chord and tarsuslength to the nearest0.1 mm, and (Marsh 1979, 1981,in press),I examined the tis- stage of molt. The molt classeswere as follows: 1 = sue energy stores and blood substrates of this no molt, 2 = light body molt, 3 = heavy body molt, speciesin samplesfrom Michigan and north- and 4 = wing and body molt. On days on which ern Florida. On the basis of its extensive more birds were collectedthan could be processed, breeding and wintering range (A.O.U. check- some of the birds collected were released after these list 1957), this species appears to be highly initial observations.Body mass and fat classwere variable in its migratory pattern. Portions of usedas indicators to help insurethat a representative the population winter in Central America and, samplewas retained. at leastin the spring,apparently migrate across On the basis of data collectedon live birds (par- the Gulf of Mexico.Lowery and Newman (1954) ticularly, body massand fat class),some of the birds were selectedfor the various proceduresrequiring reportedthe directsighting of two catbirdsover fresh muscle samples (Marsh 1979, 1981, in press). the Gulf during spring migration. Stevenson Birdsused for theseprocedures were reweighedto the (1957) lists the catbird among the trans-Gulf nearest0.01 g and immediately sacrificedby decap- spring migrants on the basis of field observa- itation. Muscle sampleswere removed from the left tions of comparativeabundance and sequence side, and the carcasseswere then placed in tightly of migration dates.In addition, catbirdswinter sealedplastic bags and stored at 4øCuntil dissection on all of the major groupsof CaribbeanIslands (seebelow). Birds used only for compositionalanal- as well as along the Gulf coast of the United ysis were sacrificedby snappingthe cervicalverte- Statesand throughoutpeninsular Florida. Small brae, reweighed to the nearest0.01 g, and stored at and variable numbers winter as far north as 4øCin sealedplastic bags until dissection.Use of the entire sample of birds for analysisof carcasscom- Long Island, New York (A.O.U. checklist1957, position required correctingwater content and lean and banding recoveriesfrom the United States dry massfor blood lost in the specimenssacrificed -banding Laboratory). by decapitation.For this purpose, the blood was es- This report concentratesmainly on the com- timated to be 80% water and 20% lean dry mass ponentsof the carcassexclusive of the flight (Altman and Dittmer 1961), and the water content muscles,which are treated separately(Marsh and lean dry mass of the carcasseswere corrected in press). The term "carcass" here refers to the appropriately(see below). body minus the two major flight musclesand Carcasscomposition.--The birds were dissected the heart. The fat content of the carcass has been within 24 h of sacrifice.The flight muscles(pectoralis measured in order to determine whether or not and supracoracoideus)were removed and weighed to the nearest 0.1 mg. (The compositionof these the amount stored is consistentwith the hy- muscleswas analyzed separately; Marsh in press).The pothesis that some catbirds cross the Gulf of body cavitywas opened,the heart removed,and sex Mexico during the fall migration. The plasma identified by examinationof the gonads.The ovaries and tissue levels of fats and carbohydrates were also removed from females in May and June measured here provide insight into the meta- and weighed to the nearest 0.1 mg. The digestive bolic stateof theselong-distance migrants. Ad- tract was left intact, becausepreliminary data indi- ditionally, this detailedcompositional analysis catedthat the 1.5-2 h that elapsedbetween collection providesthe backgroundnecessary for analyz- and sacrificewere sufficient to empty the stomach and largely to clear the remainder of the digestive ing the premigratory changesin the mass of tract. Birds were classedas juvenile (first year) or the flight musclesseen in this species(Marsh adult, basedon the pneumatizationof the skull.The in press). dissectedcarcass (the body minus the pectoralis and 172 RICHARDL. MARSH [Auk, Vol. 100

supracoracoideusmuscles and the heartand, in May- Statistics.--All statistics were determined with the Junebirds, the ovaries)was weighed to nearestmil- aid of "Midas," the statisticalprogram developed by ligram, and the partswere frozenin plasticbags and the University of Michigan StatisticalResearch Lab- stored at -20øC. Care was taken to minimize losses oratory (see Fox and Guire 1976). Comparisonsbe- duringdissections, particularly from the muscles. The tween means were made using the Student's t-test differencebetween the body massbefore dissection except between groups that had unequal variances and the sum of the massesof the parts after dissec- or small samplesizes, for which the Mann-Whitney tion was assumedto representonly water, and this U-test was used. Where parametric statisticswere amount was added to the water content of the carcass used, the meansare reportedplus or minus the stan- (water lossduring dissectionwas relativelysmall, dard error. amountingto 0.266 + 0.019 g; mean + SE). After storagein the freezer for 1•5 months, the RESULTS carcasses were freeze-dried to constant mass and re- weighed to the nearestmilligram to determinethe Bodymass and carcasscomposition.--The body dry mass.The differencebetween the freshmass and mass of the catbird varies considerably at all the dry massequals the water content.The dried seasonsof the year [Fig. 1A, Table 1 (see also carcasseswere choppedwith scissors,placed in cel- Raynor 1979)].Maximum body massis attained lulose extraction thimbles, and extractedfor 24 h with during the fall migration in Florida, although petroleumether (B.P. 30-60øC)in a Soxhletappara- many birds capturedthere still have low body tus. After extraction the carcasses were redried to masses(range 30-51 g). As the data in Fig. lB constantmass in an oven at 90øCand reweighed to indicate, much of the variation in body mass obtainthe leandry mass.The differencebetween the reflects variation in the fat content of the car- dry massand the lean dry massequals the fat (neu- tral lipid) content. cass.(Recall that in the presentcontext, the term Plasmaglucose and free fatty acidsand tissueglyco- "carcass"refers to the body minus the flight gen.--A sampleof birds was collectedin Florida to musclesand the heart and, in females during determine the concentrationof plasma glucose and May and June, the ovaries.)This relationship free fatty acids and liver and muscleglycogen con- is perhaps better illustrated in Fig. 2, which tents. An attemptwas madeto have thesesamples indicatesthat fat contentof the carcassand body reflect the substratelevels in normally active, free- mass vary in a linear fashion (r = 0.81, P < living birds. Birds were sacrificedby decapitation 0.0001, n = 95). It is also dear, however, that within 30-60 s after they enteredmist nets placed considerable variability occurs in the other near a naturally occurringfood source.Blood was collectedin small,chilled plastic beakers containing componentsof the body mass (water and lean sodium oxalateas an anticoagulant,and pectoralis dry). The water contentof the carcassis closely muscleand liver sampleswere quicklyremoved and correlatedwith the lean dry mass(r = 0.79, P < frozen in a bath of ethanol and dry ice. Blood sam- 0.0001, n = 95). Neither of these components pleswere transferredto testtubes and storedon ice. varies in any systematicway with fat content The frozen muscleand liver sampleswere wrapped (P • 0.05). in aluminum foil and stored on dry ice. Upon return The lean dry mass of the carcassis weakly, to the laboratory(within 2 h), the bloodwas centri- but highly significanfiy,correlated with the two fumedand the plasmastored frozen at -20øC for fu- linear measuresof body size: wing length (r = ture analysisof glucoseand triglycerides.Blood col- 0.37, P = 0.0002,n = 95) and tarsuslength (r = lectedby decapitationis probablymost representative of arterial blood due to bleeding from the carotid 0.31, P = 0.0026, n = 95). Other variables arteries.The frozensamples of muscleand liver were measured in this study that are significantly weighed and storedfrozen at -20øC until analysed correlatedwith the lean dry massof the carcass for glycogencontent. Glucose was determinedby a are time of capture, age, and ovary mass in modificationof the glucoseoxidase method (Sigma springfemales. The lean dry masswas elevated Chemical Co., Bulletin #510) from 0.05-ml samples in birds capturedin the evening(Fig. 3). Anal- of plasma. Plasma triglyceride content was deter- ysis of covariancedemonstrates that, although minedby calculationfrom totaland free glycerol con- the slopes of the relationships between lean tents. Glycerolwas determinedby the method of dry massand wing lengthin morningand eve- Eggsteinand Kuhlmann(1974) from 0.1-ml samples of plasma. Frozen tissue sampleswere thawed in ning birds are not significanfiydifferent, the chilled0.06 N perchloricacid, homogenized in a glass- elevations are (P = 0.002). Juvenile catbirds in glasshomogenizer, and glycogenwas determined by the fall sampleshad a significantlysmaller mean the amyloglucosidasemethod of Kepplerand Decker wing lengththan adults(86.59 + 0.24 mm and (1974). 89.09 + 0.63 mm for juveniles and adults, re- January1983] GrayCatbird Body Composition 173

50- [A] BODYMASS •45-

A A

O

O A œ A O % o o o o oooø 3C I '" I

[B] FAT

• 4

¸ A >, I¸ ,, [C] LEANDRY

Q• • %0 o o

o '-.9 5 6 7 8 9 10 Month

Fig. 1. Seasonalvariation in body mass(A), car- cassfat content (B), and carcasslean dry mass (C) in the Gray Catbird. ¸,/• = birds capturedin Michi- gan; ß = birds capturedin Florida;• = springand early summer females.

spectively;P = 0.0001for Student'st-test). The fall juvenilesalso had significantlysmaller lean dry massesthan did the adults(mean = 8.94 g vs. 9.24 g; P = 0.0304for the Mann-Whitney U-test). Multiple correlation analysis, how- ever, indicates that if the effects of size (wing length) are accountedfor, no significantage- related differences in lean dry mass remain. The lean dry massof the carcassdoes not ap- pear to be relatedto molt, season,sex, or place of capture(Michigan vs. Florida).(ANOVA and analysesof covarianceP >>0.05 in all cases.) This was despitethe factthat maleshave a sig- nificantlygreater mean wing length (Table 1; 174 R•C•4ARDL. MARSh4 [Auk, Vol. 100

16-

Catbird r= 0.81

12-

ß ß ßß oo ß ß ß ß ß ß ß ß ß ß ß ß ßßoøß ß ß ß ß ß ß ß .% o•ll** . * ß ß ß ß ***** ß * ß ß 0 I t I ' I t I ' 30 38 50 5/, Body Mass, g Fig. 2. Carcass fat as a function of body mass in the Gray Catbird.

male vs. female, total sample, P = 0.0012). In and muscle glycogen, plasma glucose, and breeding females a significant positive rela- plasma triglyceridesfor the group of birds sac- tionship exists between the lean dry mass of rificed in the field in Florida. Plasma concen- the carcassand ovary mass(r = 0.96, n = 6 for trations of glucose and triglyceride show no log ovary mass correlatedwith log lean dry significant difference (Mann-Whitney U-test) mass). In contrast, the lean dry mass does not between morning- and evening-caughtbirds. change significantlybetween May and June in Plasma glucoseshows little variation, with an male catbirds. overall mean of 3.36 + 0.15 mg/ml. Plasma tri- Tissueglycogen and concentrationof substrates glyceride glycerol, on the other hand, is ex- in plasma.--Table2 shows the values for liver tremelyvariable, with valuesranging from 1.77

TABLE2. Plasma and tissue substratesin the catbird during fall migration. Values given are the means with the sample range in parentheses.

Plasmaglucose PlasmaTGG • Liver glycogen Muscleglycogen Time (mg/ml) (/•mole/ml) (mg/g) (mg/g) Morningb 3.28 4.34 18.9 4.08 (2.79-3.74) (1.77-7.86) (3.4-36.2) (0.2-10.7) Evening •' 3.43 6.23 77.1 19.9 (3.15-3.77) (4.14-8.94) (60-103) (2.7-34) P'• 0.40 0.063 0.004 0.03 (NS) (NS)

"TGG - triglycerideglycerol. b n - 5, capturetime 0710-1040EST. c n - 6, capture time 1730-1806 EST, d Probabilitythat the morningand eveningvalues are significantlydifferent using the Mann-WhitneyU two-tailedtest. January1983] GrayCatbird Body Composition 175

Catbird o = evening ß = morning

l0 o

o

7 I I t ] I I I I ß I .I 82 8t• 86 88 90 92 Wing Length, mm Fig. 3. Leandry massas a functionof wing lengthin Gray Catbirds.¸ = birds capturedin the evening; ß = birds captured in the morning.

to 8.94 Fmole/ml.Glycogen values are four to hypothesisthat part of the catbirdpopulation five times higher in the evening than in the migratesacross the Gulf of Mexicoin the fall. morning (Table 2). Although the birds cap- Catbirdscollected in Floridahave a muchhigher tured varied in fat contentfrom approximately maximum fat contentthan Michigan birds (Fig. 1 g to greaterthan 12 g, neitherthe bloodsub- 1). This pattern of higher fat content in indi- stratesnor the tissue glycogenlevels showed viduals collectednear the Gulf is typical of oth- any significantcorrelation with the amount of er trans-Gulfmigrants (Caldwell et al. 1963). fat. I have estimated the amount of fat required by catbirdsto crossthe Gulf basedon the for-

DISCUSSION mulae of Pennycuick(1975). Although such calculationshave a strongtheoretical base and Migration patterm--Because in the present are in good agreementwith a variety of em- study of the catbird I employed discrete and pirical measurements(see Tucker 1973), they widely separated sampling locations, some may lackprecision in applicationto naturalsit- considerationmust be given to the overall mi- uations. For example, it is typical to calculate gratorypattern of the species.On the basisof "still-air" range,whereas it is clearfrom direct available banding returns and the known win- observationsof migrants that they take advan- tering areas (A.O.U. checklist1957), popula- tage of favorableweather conditionsto maxi- tions of catbirds from all parts of the breeding mize range (Lack 1960,Drury and Keith 1962, range appear to be highly variable in their Williams et al. 1977).Conversely, migrants may wintering localities. It is obvious that the cat- encounter adverse weather in the course of mi- bird as a speciesdoes not fit clearlyany one of gration,such that fat reservesare depleted and the usual classificationsof migrants according they are forcedto land short of their destina- to migratory pattern (see Helms and Smythe tion (see,for example,Johnston 1968, Williams 1969, King 1972). The sampling locations are et al. 1977). Given the possibility of errors in suchthat the fall samplesprobably contain both both directions, still-air range may provide a premigrantsand intramigrantsin Michigan and reasonablestandard for comparisonif the pos- intramigrants and postmigrantsin Florida. sible errors are kept in mind. Carcassfat content.--The data on fat content These calculations for the catbird indicate that collectedin this study are consistentwith the approximately8 g of fat would be required to 176 RICHARDL. MARSH [Auk, Vol. 100 fly from northern Florida to the Yucatan Pen- studies considering the relationship between insula, a distance of 1,000 km. Of the catbirds protein content and breeding should consider collectedin Florida, 13% had more than 8 g of the protein content of the whole and not fat. However, the actual percentageof the cat- just the flight musdes (cf. Jonesand Ward 1976, birds migrating through northern Florida that Fogdenand Fogden1979). make a long overwater flight may be much In the catbirdssampled, migratory fattening greater.Fry et al. (1970)have suggested,on the does not influence the lean dry mass of the basis of their work on trans-Saharanmigrants, carcass.These data appear to confirmthe sug- that long-distancemigrants depart soon after gestionsof Odum and colleagues(Connell et reachinghigh levels of fat. The continuingde- al. 1960, Odum et al. 1964, Rogersand Odum parture of the fatter birds means that the birds 1964)that birds showhomeostasis in otherbody sampled will be distributed in the lower fat componentsduring the addition of fat. One categories.Also, in the Floridacatbirds fat con- must also, however, considerthe data in light tents are higher in the evening than in the of the significantrelationship between lean dry morning, and 30% of the evening birds col- mass of the pectoralismuscles and fat content lected have greaterthan 8 g of fat. The overall (Marsh 1979,in press).In the catbirdand several distribution was skewed by the greater col- other species,these major flight musdes ap- lectingeffort in the morning. As Johnston(1966) parently increasein mass with incrementsin suggests,caution must be usedin inferring po- total body mass (see also Marsh and Storer tential migratorydistance from fat contentwhen 1981).This hypertrophyis consideredto be an one is collectingbirds in the processof migra- adaptation to the increased power require- tion. ments for flight. The carcasslean dry mass of Lean dry massof the carcass.--Thelean dry the remainder of the animal, however, is so massof the carcass(carcass = body of the bird variable in catbirdsthat the significantchanges minus the flight musclesand heart) is quite in the lean dry massare not evident if one at- variable in catbirds collected at all seasons and tempts to correlate the lean dry mass of the stagesof fattening (Fig. 1). As has been shown entire bird (the sum of the lean dry massof the for other small (Connell et al. 1960, carcassas defined here and the lean dry masses Rogersand Odum 1964),some of thisvariation of the muscles) with the fat content. Thus, it can be explained by variation in structuralbody may be possibleto reconcilesome of the con- size. This size-related variability is indicated flicting reports in the literature concerning by the correlation with the linear measure- whether or not body componentsother than ments of body size (wing length and tarsus fat changeduring premigratoryfattening (see length). The smaller size of the juveniles col- discussionin Fry et al. 1970, 1972).The detec- lected in the fall also appears adequate to ex- tion of a significantrelationship between the plain the age-related differencesin lean dry total lean dry mass and the fat content may mass. Beyond the correlationswith size and depend on a low amount of variability in the age there are only two factorsmeasured in this lean dry componentsexclusive of the flight study that affectthe lean dry masssignificant- muscles. ly. One factoris the time of day, with evening Tissueglycogen and bloodglucose levels.--The birds having elevatedlean dry masses(Fig. 3). levelsof tissueglycogen found in catbirdscap- Other small passerinesshow similar diurnal tured in Florida suggestthat glycogenlevels cycles,and these cycleshave been ascribedto are not suppressedduring the fall migration in a daily cycle of protein content (see Newton this species(Table 2). In fact, the concentra- 1968). The other factor is the breeding status tions of liver and musde glycogenfound in of the females. Two heavy femaleswere col- birds collectedin the evening are among the lectedin May, and they possessedlarge ovaries highest values reportedfor any passerinebird with numerous ripening follicles.The lean dry (see Farner et al. 1961, John and George 1965) masses of these females were elevated consid- and are within the range reported for man and erably abovethe remainderof the May and June captive birds and mammals (Hazelwood and sample (Fig. 1C). This large differencewas in- Lorenz 1959, Lamb et al. 1969; Baldwin et al. dependentof the flight muscles,which were 1973, Keppler and Decker 1974). The diurnal in fact smaller than expected on the basis of cyclesof glycogenfound in the catbirds also body mass (Marsh in press). Clearly, future appear to conform to data from laboratory January1983] Gray CatbirdBody Composition 177

studies.Decreases in liver glycogenduring the during migration is not known. Evidence inactive phase of the daily cycle have been availableon catabolicenzymes in the pectoralis found in birds and mammals(e.g. Hazelwood muscles of catbirds (Marsh 1979, 1981) indi- and Lorenz1959, Bonney et al. 1973).Although catesthat the ability to oxidize FFA increases lesswell studied, daily fluctuationsin muscle during fattening. This may representan ad- glycogendo occurin skeletalmuscles (Pessacq aptation that spares carbohydrateand helps and Gagliardino 1975, Conlee et al. 1976). The maintain carbohydratehomeostasis. Also, the largestcycles have been found in high oxida- lack of variation in the concentration of blood rive skeletal muscles(Conlee et al. 1976), and glucose found in catbirds (Table 2) indicates the pectoralmuscles of catbirdare very high in precise regulation of this parameter in nor- oxidative capacity(Marsh 1979,Marsh 1981). mally active, wild birds. Of course,my sam- The high glycogenconcentrations and sub- pling procedureswould not have detected the stantial diurnal fluctuationsin glycogenlevels sort of complexseasonal and diurnalcycles de- in the catbird are in agreementwith data on scribedby Dolnik (1973)using caged birds. Be- several Indian passerines(see George and cause of the limited conclusions that can be Chandra-Bose 1967) and on fall Gambel's drawn from measurements of concentration White-crownedSparrows (King et al. 1963).In only, the measurementof ratesof carbohydrate regard to conflictingreports (see Farrier et al. use in birds during various stagesof the an- 1961, Baggott 1977), it should be noted that the nual cycle is necessarybefore further conclu- lability of glycogenstores necessitates care in sionscan be drawn concerningthe importance the design of capturemethods and sampling of carbohydratemetabolism for migratory procedures,if glycogenconcentrations are to species. reflect levels present in field . Even if substantialvariability existsin glycogenstor- CONCLUSIONS age among migratory species,however, it re- mains to be determined whether these varia- Data on fat content are consistent with the tions represent intrinsic differences in the hypothesisthat a portion of the population of regulation of carbohydratemetabolism or are catbirds migrates acrossthe Gulf of Mexico due to extrinsic factors, such as diet. during the fall migration. Calculationsof mi- The importanceof carbohydratein the me- gratorydistance based on aerodynamictheory tabolismof smallpasserine migrants is difficult indicate that 13% of the birds collected had to assesson the basis of available data. Gly- accumulated sufficient reserves to cross the cogen is quantitatively unimportant in terms Gulf. Due to sampling biases, it is likely that of energystorage in theseanimals (this study, a larger proportionof the populationactually Farrier et al. 1961), but this does not mean that makes the crossing. maintenanceof carbohydratehomeostasis is not In contrast to the data on fat content, the lean critical during migration. Indeed, in mammals dry mass and water content of the carcass,ex- the maintenanceof blood glucoseand muscle clusiveof the flight muscles,do not changesig- glycogenconcentrations is crucial during pe- nificantlyin the premigratoryperiod. The flight riods of high substrateturnover such as exer- musclesdo increasein size during fattening cise and cold stress(Bergstr6m and Hultmann (Marshin press),however, which is interpreted 1967, Saltin and Karlsson 1971, Minaire et al. as a specificadaptation of thesemuscles to com- 1973, Paul and Holmes 1975), even though fat pensate for increasesin the power require- is quantitativelythe most importantsubstrate. ments for flight. These data, combined with In these mammals, the turnover and oxidation information on a more limited sample of of plasmaglucose are elevatedin proportionto breeding females,clearly indicate that the lean the increase in metabolic rate, and the duration dry mass of the flight musclesand of the re- of exercisemay be limited by the ability to mainderof the body do not necessarilychange supply this glucose.Additionally, Marsh and in concert.Therefore, studies consideringthe Dawson (1982) have suggestedthat carbohy- importanceof protein in the annual cyclesof drate may be the limiting fuel for thermogen- birds should consider changes in the entire esis in the American Goldfinch (Carduelistris- body and not just the flight muscles. tis). Whetheror not this informationapplies to Field samplesduring the fall migratory pe- the high metabolicrates that must be sustained riod demonstratethat tissueglycogen levels are 178 RICHARD L. MARSH [Auk, Vol. 100 not suppressed during migration in this variationand effectsof fasting.Amer. J. Physiol. species. More information on the concentra- 231: 614618. tions and kinetics of carbohydratesis neces- CONNELL, C. E., E.P. ODUM, •: H. KALE. 1960. sary before the role of these substratesin mi- Fat-free weights of birds. Auk 77: 1-9. DOLNnC,T. V. 1973. [Diumal and seasonalcycles gratorybirds can be clarified. of the blood sugarin sedentaryand migrating birds.] Zool. Z. 52: 94-103. ACKNOWLEDGMENTS DRURY,W. H., & J. A. KEITH. 1962. Radar studies This studywas supportedprincipally by NSF grant of songbirdmigration in coastalNew England. DEB 76-21376for support of doctoralresearch and a Ibis 104: 449489. dissertationgrant from the Horace H. RackhamSchool EGGSTEIN,M., & E. KUHLMANN. 1974. Triglycer- of Graduate Studies. Additional logistical support ides and glycerol:determination after alkaline camefrom NSF grant DEB 77-25487to W. R. Dawson. hydrolysis.Pp. 1825-1831in Methodsof enzy- Support during the preparationof this report, was matic analysis,vol. 4. (H. U. Bergmeyer,Ed.). derived from NSF grant PCM 81-02331to A. F. Ben- New York, Academic Press. nett. W. R. Dawson provided space,equipment, crit- EVANS,P.g. 1969. Ecologicalaspects of migration, icism, and encouragementthroughout this study. D. and pre-migratoryfat depositionin the Lesser W. Johnstonprovided spacein his laboratory and Redpoll, Carduelisfiammea cabaret. Condor 71: solvednumerous logistical problems during my stay 316-330. at the University of Florida. J. A. Faulkner, K. F. leARNER,D. S., J. g. KING, & M. H. STETSON.1968. Guthe, and R. W. Storer provided commentson an The controlof fat metabolismin migratorybirds. earlyversion of this report.S.J. Wickletkindly helped Proc. 3rd Intem. Congr. Endocr.: 152-157. with the glycogenassays. , A. O•CSCHE,F. I. K•MENOTO,J. R. KINe, & H. E. CHEYNEY. 1961. A comparison of the

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