Body protein does not vary despite seasonal changes in fat in the White Stork Ciconia ciconia

Ibis (2002), 144 (on-line), E1–E10

© 2002 British Ornithologists’ Union

Blackwell Science LtdBody protein does not vary despite seasonal changes in fat in the White Stork Ciconia ciconia

DELPHINE MICHARD-PICAMELOT,1 THIERRY ZORN,2 JEAN-PAUL GENDNER,1 ASTOLFO J. MATA1 & YVON LE MAHO1*

1Centre d’Ecologie et Physiologie Energétiques, C.N.R.S., 23 Rue Becquerel, 67087 Strasbourg Cedex 2, France 2Office National de la Chasse, 85 bis Avenue de Wagram, 75822 Paris Cedex 17, France

To understand how a large soaring bird, the White Stork Ciconia ciconia, copes with energyconstraints, we compared changes in body mass in 14 captive adult storks with the bodycomposition of 12 free-ranging adult storks found dead from accidents. The captive storks,already in an enclosure for several years, were fed ad libitum. They were weighed daily for1.5–3.5 years using an automatic device. The bodies of the accidentally killed storks wereanalysed to determine total water, lipid, protein and ash contents, and to assess the bio-chemical composition of certain organs. Females were on average 20% lighter and 24% smallerthan males, but the body mass of the sexes varied in parallel throughout the year. Body masspeaked in December and January (25–30% above minimal body mass), due essentially tolarge fat stores in subcutaneous and abdominal adipose tissues. Body mass and body lipidrapidly decreased from February to June, whether the storks reared chicks successfully ornot, and remained minimal for a few days into July. In contrast to birds using flapping flight,no variation in body protein or pectoral muscle protein was observed while breeding, eventhough the moult occurred then, nor in August, before the time when wild storks migrate.An endogenous regulation of body fuels is discussed.

Changes in a bird’s body mass largely reflect modifica-tions in the ratio of energy intake/energy utilization.Through the seasons, life history events and endogen-ous programming influence the energy demand andintake in such a way that regular variations in bodymass may occur (Blem 1990, Gwinner 1990). Bodymass varies most during reproduction and migration.Final reproductive success sometimes depends onbody mass at the onset of breeding (capital breeders,Drent & Daan 1980), the importance of the drop inbody mass during breeding thus reflecting the invest-ment of parents in chick protection and feeding. There-after, during migration, the energy demand can beextremely high (Lindström & Piersma 1993, Bairlein& Gwinner 1994), while there is no opportunity toforage. The birds anticipate these energy demands byincreasing their stores of ‘body fuels’ (Berthold 1974,Blem 1990).

In birds relying on body fuels for breeding, it iswell documented that both body fat and protein are

accumulated beforehand (Robin et al. 1988, Groscolas1990, Cherel 1995). In contrast, it has, until recently,generally been assumed that for birds prior to migra-tion, the increase in body mass is essentially due tofat accretion, with the accumulation of other bodyfuels being negligible (Berthold 1974, Blem 1990,Ramenofsky 1990). However, data are now accumu-lating to suggest that there is also significant bodyprotein accumulation prior to migration (Marsh 1984,Gauthier et al. 1992, Lindström & Piersma 1993,Bairlein & Gwinner 1994, Piersma 1998). This accordswith other data indicating that not only fat, but alsobody protein, is used as fuel during migration(Jenni-Eiermann & Jenni 1991, Bairlein & Totzke1992, Bairlein & Gwinner 1994, Biebach 1998, Jenni& Jenni-Eiermann 1998, Lindström et al. 2000). Inaddition to being a further source of body proteinduring flight, its accretion in muscles prior to flightwould enable a bird to maintain optimal powerfor flying, despite the increased load from fataccumulation (Marsh 1981, 1984, Weber & Piersma1996, Biebach 1998). However, the informationavailable on changes in bird body composition pertains

*Corresponding author. E-mail: [email protected]

E2 D. Michard-Picamelot et al.

© 2002 British Ornithologists’ Union, Ibis, 144 (on-line), E1–E10

only to species that rely on flapping flight. For soaringbirds, the increased load resulting from body fuelaccumulation should be optimized differently(Pennycuick 1975, Smith et al. 1986, Hedenström &Alerstam 1998).

The White Stork Ciconia ciconia is a soaring migrant,whose Alsatian population is now mostly sedentarydue to human intervention. Based on monthlyweighings, a circannual change in body mass has beenfound in captive storks fed ad libitum (Hall et al.1987). As we have shown, this body mass cycle canbe monitored automatically in storks implanted witha transponder tag without any human disturbance(Michard et al. 1995), but no other data are yetavailable on the annual body mass cycle of storks.

Thus, the main objective of the present studywas to compare the seasonal change in body massof undisturbed captive adult white storks with thebody composition of free-ranging adult storks founddead from accidents in Alsace. Factors which mightinfluence the annual cycle of body mass and composi-tion are discussed.

MATERIALS AND METHODS

The White Stork situation in Alsace

The Alsatian population of the White Stork, a part ofthe Western European population, was saved fromextinction in the 1970s (Bairlein 1991) by keepingmany fledging storks in captivity until sexually mature(about 3 years, Bloesch 1980, Schierer 1983). Therebythey were prevented from migrating to Africa; amigration which has been considered as the maincause for a high mortality (Schulz 1995). Oncereleased and provided year-round with food at numer-ous feeding stations in Alsace, these storks becomesedentary. Their fledglings, usually thought to migrateas other wild storks do, sometimes show intermediatebehaviour, i.e. they appear to be erratic (Michard et al.1995, 1997). The proportion of free-ranging birdsshowing each of these behaviours, i.e. sedentary,erratic or migrant, is unknown.

Seasonal changes in body mass

Between 1993 and 1996, the body mass of six maleand eight female adult White Storks was recorded forbetween 1.5 and 3.5 years, depending on the indi-vidual. The storks were 5–25 years old, and werebred in an outside enclosure in Strasbourg (France).Throughout their captivity they had ad libitum

access to food (meat and vitamins) and water. In1995, the number of chicks reared was checked.

The birds, which were implanted with a trans-ponder tag, were identified and weighed as theystood on a balance to get food (for technical details seeGendner et al. 1995, Michard et al. 1995). Severalweighings were recorded daily for each stork with-out handling or disturbance.

To compare annual body mass changes amongindividuals, a cosine curve was fitted by an iterativeprocedure to the body mass (BM) data for each stork(Sigma Plot, Jandel Software):

BM = M + A · cos[2π · ( (date – D)/365) ]

where BM (g) and date (days) are known values.Three free parameters were then determined: M =mean BM (g); A = amplitude of BM variation frommean BM (g); D = interval from 1 January to themaximal BM (days).

Body composition

Owing to the protected status of the White Stork inFrance, a permit was obtained to collect 12 free-ranging adult storks which had died accidentally inAlsace from 1992 to 1996 (licences 92/176, 93/627,94/515B and 96/054 from the Ministère français del’Environnement). These birds were victims of electro-cution, or collisions with power lines or cars. One storkwhose death could be attributed to a pathologicalcause was excluded from the study. Because of theprovision of feeding stations in Alsace, none of thebirds was emaciated.

Seven of the storks accidentally killed had beenringed, which enabled their origin and age to be known,and for four of them, also that they were non-migratory.The other five bore no identification, indicating thatthey had never been in captivity. Their origin, ageand migratory status are unknown. Their maturity wasdetermined by the absence of a bursa of Fabriciusand by the full red coloration of bill and legs.

Sometimes the storks were discovered manyhours after death and at times brought to us underuncontrolled transport conditions, often already frozen.Partly decomposed bodies were excluded from thisstudy. The birds selected were preserved in plasticbags at –20 °C. Because of possible evaporation, thefresh body mass (FrBM) was recorded as soon aspossible, but was considered to be an approximationto the mass of the live individual.

To determine the body composition, feathers andgut content were first removed. All the muscles from


Seasonal changes in body condition of the White Stork E3

the left leg, left side pectoral muscles (pectoralismajor + pectoralis minor), heart, liver, empty digestivetract, abdominal adipose tissue, and subcutaneousadipose tissue and skin (SCAT + skin) were removed.The skeleton and remaining tissues were consideredas the carcass. Each organ was weighed to the nearest0.1 g, cut into small pieces and lyophilized to deter-mine its dry mass. The dry body mass (DryBM) wasobtained by pooling the dry masses of each organ.Organs were then ground into fine powder and con-served at –20 °C in hermetic boxes until determina-tion of lipid, protein and ash contents.

In order to determine the body fuel content of thebirds, the lipid content was evaluated by an extractionmethod adapted from Folch et al. (1957) on about2 g of each dry organ with chloroform/methanolsolvent. The protein content, representative of muscleor connective tissues, was determined using theKjeldahl method for nitrogen on 35–130 mg of eachdry organ. The ash content, which reflects the mineralfraction, was measured by heating 2–5 g samples at800 °C for 24 h in a muffle furnace.

The body lipid mass (BLip), body protein mass(BProt) and body ash mass were obtained by poolingthe dry contents of lipid, protein and ash of eachorgan. Three leg samples were inadvertently lost dur-ing the lyophilization procedure. Their contents ofwater, lipid, protein and ash were taken as the meansof other leg results for reconstitution of the bodycomposition, but were not included in organ results.

Skeletal ash content (SkAsh) was approximatedby carcass ash content minus breast muscle and totalleg ash contents, the mineral content of remainingsoft tissues being negligible. Skeletal ash is nearlyconstant during the entire life of adult birds, but afew modifications can occur during egg laying infemales (Taylor et al. 1971), moult (Zahnd 1954)and prolonged fasting (Thouzeau 1998). Still, moult isprogressive over several months in White Storks, andin our study no female was found in the period of eggproduction, and none of the accidental deaths could beattributed to an energetic deficit. As a consequence,skeletal ash was considered to be a constant represent-ative of structural body size, related to the three dimen-sions of the animal (Piersma & Davidson 1991).

Statistical analysis

Values presented are means ± standard deviation (sd).To compare data among groups after checking fornormality and equality of variance, analysis of vari-ance (ANOVA) or covariance (ANCOVA) was performed

(Minitab software). When the distribution of the datawas not normal, the Mann–Whitney U-test was used.

RESULTS

Seasonal changes in body mass of captive storks

The 14 captive adult storks, whose body mass wasmonitored automatically, showed a regular circannualchange in body mass (see Fig. 1 for data on one femaleand one male). Body mass followed a near sinusoidalcycle, with maxima in December–January and minimain July. The maximal body mass was 25–30% abovethe minimal value. The decline in body mass, fromFebruary to late June, coincided with the breedingseason. Body mass increased slowly from late July,i.e. the time of premigratory behaviour, and thensteeply during late summer and autumn when wildstorks are usually migrating.

The cosine fit applied to the cycle of each individual(see Materials and methods and Fig. 1) allowed bodymass changes among individuals to be compared(Table 1). Females were on average 20% lighter thanmales (P < 0.05), but the amplitude of annual changesin body mass, whether relative or absolute, did notdiffer significantly between sexes. The maximum bodymasses (maxima of the fitted function) were reachedabout 13 days earlier for females (late December toearly January) than for males (mid-January, P < 0.05).The age of the storks (5–25 years), equivalent tolength of captivity when the present study started,had no influence on the parameters of the body-masscycle. Also, the five storks that had reared one ormore chicks in 1995 showed similar body masschanges to non-breeding individuals throughout thereproductive period.

General body composition of free-ranging storks

The timing of death of the 12 individuals foundallowed us to study the changes in body compositionduring the first 9 months of the year (from earlyJanuary to late September, Fig. 2 and Table 2). Bothmales and females were regularly dispatched to usthroughout that period.

Figure 2 shows the fresh body mass of the accid-entally killed storks plotted together with the cosinefunction fitted to the body mass of the heaviest andthe lightest live storks studied in captivity. Eleven ofthe 12 storks studied each presented a body mass



that fell within the range observed for their captiveconspecifics for the same period of the year. Theremaining individual was the smallest female, killed inFebruary, but which still presented an appreciableamount of fat and no sign of protein depletion.

The range in fresh body mass indicated large inter-individual variations (from 2930 to 4690 g, Table 2).Female mean fresh body mass was 19% less than formales (P < 0.005), and consequently female meandry body mass was also 18% (but not significantly) lessthan for males. This was partly due to a large variationin structural size, as shown by the range in skeletalash (from 128 to 215 g, Table 2), indicating that females

were systematically smaller than males (mean skeletalash 24% smaller, P < 0.005). Nevertheless, the largedistribution of structural sizes observed in each sexresulted in a difference of less than 3% between theskeletal ash of the largest female and of the smallestmale (respectively 169 and 174 g).

On average, females presented significantly lessbody protein than did males (P < 0.005, Table 2), andamong the two groups, body protein showed smallinterindividual variations (sd being 3 and 10% of themean for males and females, respectively). Similarly,no significant difference was found between meanbody lipid of males and females, but interindividual

Figure 1. Automatically monitored body mass (d) of two captive White Storks (upper graph, a female born in 1974, lower graph, a maleborn in 1984) from April 1993 to September 1996. Values are means of weighings for 10 consecutive days ± sd. The cosine curve wasfitted to the annual body mass variations (see Materials and methods). Hatched boxes (B): breeding period, from pairing to definitivefledging of young. Black line (M): theoretical timing of migration and wintering for free-ranging white storks.



differences of body lipid were particularly important(from 276 to 1122 g for males and from 177 to 1290 gfor females), which suggests that body lipid formeda major component of body mass variation.

Body composition related to structural size

Because of the differences in structural size repres-ented by skeletal ash (Fig. 3) observed in our bird

sample, we investigated the covariation of body com-position with size. Despite the sexual size dimorphismseen, an ANCOVA showed that males and females pre-sented similar relationships between body proteinand skeletal ash (F1,9 = 0.96, P = 0.35). In view ofthe large range of sizes in each sex, all data were thenpooled.

The strong correlation of body protein with skeletalash (r2 = 0.82, P < 0.001, Fig. 3) found for the 12 deadstorks suggests a proportional increase in structuralprotein (connective tissue and muscles) with increasingstructural size in both sexes. In contrast, there was nocorrelation between body lipid and skeletal ash(r2 = 0.003, n.s.).

In none of the various organs studied was lipidcontent correlated with skeletal ash (r2 < 0.1, n.s.throughout). But as observed for total body pro-tein, the protein content of some organs wasrelated to the structural size represented by skeletalash (Fig. 4). The protein content of leg and pec-toral muscles, and of the whole carcass, increasedwith skeletal ash (r2 = 0.63, r2 = 0.62 and r2 = 0.65,respectively, P < 0.005 for each), as did the proteincontent of subcutaneous adipose tissue and skin(r 2 = 0.63, P < 0.005). In contrast, the protein con-tent of visceral muscles such as heart or digestivetract, and also of liver and abdominal adiposetissue, were not related to skeletal ash (r2 < 0.1, n.s.throughout).

Body composition and seasons

In order to understand the annual variations in bodymass observed in the captive live storks, we investig-ated the variations in body composition of the 12

Table 1. Comparison of parameters for the cosine curves fitted to body mass for captive White Storks (n = 14). Values are means ± sd.n: number of individuals in each subgroup. An analysis of covariance was performed between the two subgroups of each category.

Category nMean body mass (g) Amplitude (g)

Relative amplitude (%)

Delay from 1 Jan. to maximal body mass (days)

Sexmale 6 4430 ± 271 489 ± 60 11.1 ± 1.4 16.7 ± 6.4female 8 3545 ± 297* 468 ± 97 13.2 ± 2.5 3.3 ± 9.6*

Age< 14 years 7 4122 ± 522 470 ± 61 11.5 ± 1.8 11.6 ± 12.3≥ 14 years 7 3727 ± 499 484 ± 101 13.1 ± 2.6 6.5 ± 8.6

Chicks reared in 1995:0 9 3849 ± 552 470 ± 71 12.4 ± 2.5 9.7 ± 11.1≥ 1 5 4060 ± 522 491 ± 104 12.1 ± 2.3 7.8 ± 10.6

*Significant difference between the two subgroups of a category, P < 0.05.

Figure 2. Fresh body mass of 12 accidentally killed White Storksat time of death (f = female, m = male). The upper cosine curvewas fitted to the body mass of the heaviest captive White Storkstudied (a male born in 1982). The lower curve, same for thelightest captive White Stork studied (a female born in 1971).



accidentally killed storks as a function of their datesof death (Fig. 5). For statistical analysis, the originaldata (full symbols on Fig. 5) were separated into(i) a ‘light body mass’ period from March to July(n = 6), and (ii) a ‘heavy body mass’ period fromAugust to February (n = 6). To take into account theinfluence of structural size, we performed a covari-ance analysis on the body component data for these

two periods, using skeletal ash as a covariate. Bodyprotein showed no significant modification with theperiod of the year (F1,9 = 0.08, n.s), but body lipidsignificantly increased during the ‘heavy body mass’period (F1,9 = 17.93, P = 0.002), in parallel with drybody mass variations (F1,9 = 5.6, P = 0.039). To

Figure 3. Body protein (j) and body lipid (s) of 12 White Storksfound accidentally killed plotted against their skeletal ash. Females(low skeletal ash) and males (high skeletal ash) are plottedtogether. The solid line is the linear regression performed onbody protein for the 12 individuals pooled (r 2 = 0.82, P < 0.001).

Table 2. Individual date of death and body composition of 12 white storks found accidentally killed. FrBM: fresh body mass. DryBM: drybody mass. SkAsh: skeletal ash. BProt: body protein. BLip: body lipid. m: males. f: females.

Sex Stork Date of death FrBM (g) DryBM (g) SkAsh (g) BProt (g) BLip (g)

m S2 early May 3620 1256 215 718 276S3 late March 4110 1363 212 763 341S4 7th September 4360 1875 174 714 933

S14 24th June 4100 1347 184 696 405S23 mid-January 4690 2135 195 751 1122

mean ± sd (n = 5) 4176 ± 393 1595 ± 387 196 ± 18 728 ± 28 615 ± 385

f S1 early May 3000 973 149 616 177S11 14th June 3280 1007 156 626 178S16 3rd July 3560 1258 169 631 406S17 24th August 3430 1239 141 573 443S20 mid-February 2930 1145 142 487 466S21 early January 4410 2133 154 626 1290S33 24th September 3170 1434 128 504 761

mean ± sd (n = 7) 3397 ± 499* 1313 ± 394 149 ± 13** 580 ± 61** 532 ± 389

*Significant difference between sexes, P < 0.05. **Significant difference between sexes, P < 0.005.

Figure 4. Protein content of carcass (e), pectoral muscle (d),subcutaneous adipose tissue and skin (SCAT + skin, ,) and legmuscle (j, three samples lost) of 12 White Storks foundaccidentally killed plotted against their skeletal ash. The solidlines are linear regressions performed on each organ proteincontent for the individuals pooled (r 2 > 0.62, P < 0.001 for each).



illustrate this phenomenon more clearly, data correctedfor structural size are also shown in Fig. 5 (opensymbols).

The adiposity, defined as the proportion of fat inthe fresh body mass, was about 27% in January, andfell to only 8% in late spring and early summer. Thecontribution of body lipid to the annual change indry body mass was investigated with a linear regression(r2 = 0.91, P < 0.05, Fig. 6). The slope of the equationobtained did not differ significantly from 1 (Student’st-test), indicating that the annual change in bodylipid was responsible for the near totality (1/slope =97%) of the absolute annual change in dry body mass.Accordingly, there was no significant correlationbetween fat-free dry body mass and body lipid(r2 = 0.009) or between body protein and body lipid(r2 = 0.008).

Abdominal and subcutaneous adipose tissueswere mostly involved in the annual change in body

lipid, since they represented 75% of body lipid inwinter and only about 20% in late spring.

In view of the apparent stability of the proteincontent of the storks throughout the year, we lookedfor evidence of an increase in the protein content ofcertain organs known to be involved in migration.For this purpose, eight individuals were selected fromour sample on the basis that their specific informa-tion indicated that they might have been migrants.The ‘post-migration’ storks (three individuals fromFebruary to May) were separated from the ‘premigra-tion’ ones (five individuals from June to September).No significant difference was found in the protein con-tent of the pectoral muscle (U = 11, P = 0.55) nor ofthe digestive tracts of these birds (U = 8, P = 0.14).

DISCUSSION

Despite a major difference in the status of the twogroups studied, one captive and one free-ranging,data for both groups showed strong similarities.First, the fresh body masses of the accidentally killedstorks matched the range of body mass observed fortheir captive conspecifics during the same period(Fig. 2). Moreover, the mean body masses of the twogroups were very similar (Tables 1 and 2). The totallipid mass loss indicated by differences betweenstorks killed accidentally between January and Julycorresponded remarkably well with the drop in bodymass of the captive live storks during the same

Figure 5. Body lipid (a, circles) and body protein (b, squares) of12 White Storks found accidentally killed as a function of date oftheir demise. Full black symbols are uncorrected data. Openwhite symbols are data corrected for structural size (normalizedto a mean skeletal ash mass of 180 g).

Figure 6. Dry body mass (DryBM) of 12 white storks foundaccidentally killed as a function of their body lipid (BLip). The solidline is the linear regression given in the upper part of the figure.



period (about 1000 g; Fig. 5 and Table 1). Similarly,the gain in body mass monitored in the captive livestorks from July to September was close to the bodylipid gain observed in the killed storks over the sameperiod (slightly more than 500 g).

Consequently, and despite the fact that no com-parison was possible from October to December whenno data were available for free-ranging storks, we canassume that the changes in body mass observed incaptive storks probably correspond to the modificationsof body composition measured on free-ranging birds.

Body size variations

Although the sexes do not seem to be distinguishablein the wild in this species, our data are the first toquantify a strong sexual size-dimorphism suggestedin the literature (Cramp & Simmons 1977, Hall et al.1987, Del Hoyo et al. 1992), since annual mean bodymass was 19–20% less, and structural size 24%smaller, in females (Tables 1 and 2).

As expected, since the mass of structural muscles isusually related to the size of the individual, the proteincontent of the whole bird, and of the carcass, pectoraland leg muscles, were closely related to the skeletal ash(our body size criterion) irrespective of the sex (Figs 3and 4). In contrast to body protein, the fact that bodylipid was independent of structural size (Fig. 3) canbe attributed to the large quantity of adipose tissuemanaged as fuel stores throughout the year, which couldmask slight variations in structural lipids with size.

Annual body mass cycle and body composition

To discuss variations in body composition, we definestores as the nutrients accumulated in anticipation ofperiods of shortage. They are different from reserves,which are used only in an emergency because theyconstitute a normal part of the body (Van der Meer& Piersma 1994). Since the storks studied in thispaper were not confronted with any food shortage dur-ing a high energy demand period, our data thereforedeal with fuel stores.

The change in body mass of White Storks ismonomodal and regular throughout the year (Fig. 1).In July, when day-length is near the maximum, thebody mass of our adult storks remained minimal fora few days (Fig. 1). Their body mass then increasedsteadily and rapidly with increasing night-length,and in early winter the maximum body mass was25–30% above the minimum. These results suggest

that photoperiod variations may be involved in aprogramming of annual changes in body mass, asobserved in many bird species (Gwinner 1990). Datafrom storks wintering under tropical day-lengthwould be interesting to test this hypothesis.

We observed that the reproductive success of pairsdid not influence the individual body mass variation(Table 1). Consequently, the high energy requirementsof rearing offspring (Drent & Daan 1980), even ifpartly implicated, cannot be considered the main causeof the springtime drop in mass observed.

It has been observed under ad libitum conditionsthat captive adult storks spontaneously decreasetheir food intake in spring to less than half that ofwinter (unpublished data). This drop in food intakecould then be the basis of the decline in body massin spring, as has already been supposed for this species(Hall et al. 1987) and observed in some fasting breed-ing birds (Mrosovsky & Sherry 1980). The drop ofbody mass would thus be endogenously programmed.

As in most other birds (Pond 1978, Blem 1990,Bairlein & Gwinner 1994), the White Stork stores lipidsprincipally in subcutaneous and abdominal adiposetissues (50 and 25% of total body lipid, respectively).But unlike several other species that have been studied,no protein accumulation is involved in the bodymass increase of the storks (Figs 5 and 6). This resultcontrasts with the assumption of Hall et al. (1987)that body mass changes of the White Stork are linkedto muscle mass variations.

As a consequence, the decrease in body mass inspring is explained by the utilization of large amountsof lipid only (Figs 5 and 6). Indeed, even duringreproduction and moult, the protein content ofpectoral muscles and total body protein remainedconstant despite loss in body mass (Fig. 5). This obser-vation contrasts with numerous bird studies that giveevidence for body protein loss during moulting(Milne 1976, Reinecke et al. 1982, Mainguy & Thomas1985, Blem 1990) and for females during egg laying(Milne 1976, Mainguy & Thomas 1985, Blem 1990,Choinière & Gauthier 1995, Houston et al. 1995). Thepattern in storks, however, could also be explained bysufficient protein intake via alimentation, since storksare exclusively carnivorous (Del Hoyo et al. 1992).

In agreement with the hypothesis of an endogenousregulation of body mass, captive and free-rangingstorks showed a similar pattern of body mass variationfrom January to September. Nevertheless, to ourknowledge there are no existing data to indicate thatmigrant storks might fatten in the same way, especiallyduring the last three months of the year when they



reach tropical areas. A longer period of high bodymass in winter has been observed in some cagedbirds compared to wild conspecifics, and this hasbeen linked to their reduced energy expenditure andenvironmental stimuli (Bairlein & Gwinner 1994).Long-term captivity has been proposed recently tomodify the annual hormonal cycles of migrating birds(Piersma & Ramenofsky 1998), and thus potentiallythe body mass cycle. Therefore, to compare the accu-mulation of stores and their utilization during autumn,the natural migration period, it would be interestingto study the changes in body mass and compositionof migrant storks on their African wintering areas.

A special aspect: body composition and soaring migration requirements

The physiological implications of migration havebeen investigated largely in birds such as passerines oranatids that use flapping flight (Berger & Hart 1974,Berthold 1974, Lindström & Piersma 1993, Bairlein& Gwinner 1994), or have been modelled (Weber et al.1998). In contrast, little is known about the cycle ofnutrient stores of soaring birds (Smith et al. 1986).

If wild storks show similar body mass variations toour sedentary ones, they would leave their breedinggrounds in September with a body mass still close tothe minimal value (Figs 1 and 5) and their annualcycle would be monomodal. This contrasts with theusual body mass variation in migrant birds, which showspeaks of body mass before the two annual migrations(Berthold 1974, Blem 1990). This observation couldbe related to the fact that the energy requirementsof soaring flight are relatively low, since storks glideon rising thermals (Berger & Hart 1974, Pennycuick1975). Soaring flight requires night stopovers afternearly daylong journeys (Pennycuick 1975), whichalso allow the storks to rest and forage every 300–400 km (Leshem & Yom-Tov 1996), unlike certainsmall birds that rely exclusively on body fuels duringlong-distance non-stop flapping migration (Berthold1974, Blem 1990, Bairlein & Gwinner 1994). Thus forstorks, fuel stores need not necessarily be large at depar-ture, a fact which would favour the birds’ aerodynamics(Pennycuick 1975, Hedenström & Alerstam 1998).

In the same way, if the absence of protein accre-tion in sedentary storks during summer also occurs inwild storks prior to migration (Figs 5 and 6), it woulddiffer from flapping birds which are known toaccumulate proteins via muscle optimization whenboth larger fat loads and high flight power requireenhanced muscle capacity (Bairlein & Gwinner 1994).

CONCLUSION

We report here, for the first time, data on body com-position variations over the annual body mass cyclein a large soaring bird. The regular sinusoidal bodymass cycle is exclusively due to high lipid storage andcatabolism throughout the year. We demonstratean absence of variation in the protein content of thestorks throughout the year, despite large changes inbody mass, and particularly no hypertrophy of pectoralmuscles prior to the theoretical migration period.These results are consistent with the hypothesis ofan endogenous optimization of body compositionthroughout the seasons, but additional data are nowrequired to ascertain whether the annual manage-ment of body fuels is similar in wild migrant storks.

This work has benefited from grants from the ‘Ministère del’Environnement’ and the ‘Région Alsace’. We thankA. Ancel, J.-C. Clauss, T. Clauss, L. Gangloff, H. Heijkoop,A. Pape, C. Rink, J.-P. Robin, G. Wilmann and members ofour laboratory for technical help and scientific discussions.

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Received 3 August 2000, revised manuscript accepted 16 July 2001

Body protein does not vary despite seasonal changes in fat in the White Stork Ciconia ciconia

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