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AMER. ZOOL. 16:671-684 (1976). Patterns of Lipid Storage and Utilization in Birds CHARLES R. BLEM Department of Biology, Virginia Commonwealth University, Richmond, Virginia 23284 SYNOPSIS Nowhere among the vertebrates does the capability for storing and using triglycende as an energy reserve exceed the level found in the class Aves. Adult avian depot fats are composed largely of 16- and 18-carbon fatty acids and are mostly unsaturated. Variation in fatty acid composition among species may be attributed to dietary differences and physiological state of the bird. Storage occurs mainly by addition of lipid to adipocyte vacuoles without an increase in cell number. Daily cycles of fat deposition and use are of greater amplitude at higher latitudes, but in general the lipid stored during the day will only provide energy for the overnight fast plus a few daylight hours. Storage levels may be minimized due to the disadvantages of increased wing-loading. A variety of behavioral, physiological and morphological adaptations may be used to reduce the need for overnight energy reserves. Migratory fattening is largely a function of migration speed, magnitude of barriers to be crossed and aerodynamic considerations. Lipid reserves are greatest in eggs of precocial birds and are retained longer in precocial young. Adaptive strategies of fat deposition in young birds are related largely to the ability of adults to feed young before and after fledging. INTRODUCTION It is axiomatic that organisms capable of storing appropriate amounts of energy will have a selective advantage during those times in their lives when energy demands are great. Nowhere among the vertebrates does the rate of storing and using energy exceed the level found in the class Aves. Energy is stored largely as lipids, particularly triglycerides. Most birds, including many of the smaller species, generally do not feed after dark and therefore must deposit lipids to provide energy for an overnight fast. In House Sparrows, Passer domesticus, a permanent resident, this lipid may amount to 14% or more of fat-free fresh body weight in midwinter at northern sites (Blem, 1973). Storage is even more striking in migrants as some small species (including the tiny Ruby-throated Hummingbird, ArI am grateful to L. B. Blem, D. W. Johnston, S. C. Kendeigh,J. R. King, and J. F. Pagels for constructive criticism of the manuscript. Mary White and M. A. Byrd provided copies of pertinent references. The preparation of the paper was partly supported by the Department of Biology of Virginia Commonwealth University and original research reported in this paper was partly supported by a Virginia Commonwealth University faculty research grant. chilochus colubris) make nonstop migratory flights of 1,000 km or more across the Gulf of Mexico (see Odum et al., 1961; Odum, 1965) and several species deposit more than 40% of their body weight in premigratory fat (Odum and Connell, 1956; King and Farner, 1965). Probably all young birds must carry lipid reserves at fledging sufficient to maintain them until they can forage for themselves. In young Gannets, Mortis bassanus, this reserve may amount to 1,000 g of fat (Nelson, 1966) or about onethird of the adult weight. The following review is limited primarily to the biology of storage and use of triglycerides in wild birds, and the adaptive relationship of such energy stores to avian life histories. Much of the research described in this report involves only a few species of finches. Because of the restricted phylogenetic nature of these birds, many of the following conclusions probably should not be applied to other groups of birds (King and Farner, 1965). FATTY ACID COMPOSITION OF AVIAN LIPIDS Techniques for extraction of avian lipids for studies of fatty acid composition are 671 TABLE 1. Majorfatty acids in nonmigrating birds. (Values are percentages of total extracted lipids.) Carbon atoms: Double bonds Species Adelie Penguin" Takahe Herring Gull Skua Gull Gannet Fulmar Willow Ptarmigan6 Willow Ptarmigan Rock Ptarmigan0 Rock Ptarmigand Red Grouse" Black Grouse" 14:0 16:0 16:1 18:0 18:1 18:2 18:3 6.1 14.8 25.1 18.5 16.4 17.1 13.9 13.022.0 17.4 21.4 15.0 12.0 21.6 16.4 11.813.4 11.4 23.8 11.7 26.3 27.8 29.437.5 31.233.7 16.6 20.1 8.5 3.6 3.4 6.2 5.7 3.6 3.2 31.7 61.7 3.7 4.3 1.0 5.011.0 11.5 10.017.0 15.4 29.8 3.3 1.9 3.2 2.0 0 Nov. May Capercaillie" Great Tit e Redpoll House Sparrow House Sparrow' Dark-eyed Junco White-throated Sparrow W S 6.4 Jan. Aug. W 3.1 4.0 4.6 5.2 3.9 2.04.0 1.8 4.0 2.3 2.7 1.7- 2.0 6.0 8.5 7.0 7.1 3.99.5 3.46.0 2.6 3.0 9.1 5.0 5.0 7.5 5.6 4.27.3 16.0 12.7 5.8 11.0 13.8 9.217.7 11.416.1 7.1 10.1 8.0 9.0 51.3 33.6 6.014.9 16.9 35.1 29.9 25.939.9 23.625.9 29.2 27.3 30.5 32.6 28.3 26.9 30.044.0 40.2 22.7 25.0 29.0 13.8 28.9 19.624.5 72.0 57.5 48.4 11.5 15.8 7.611.5 13.716.8 38.6 32.8 20:1 20:4 5.2 20.3 19.7 24.2 26.8 22:5 22:6 2.1 8.6 16.5 18.5 17.4 22.1 12.026.0 11.3 10.0 35.0 32.0 Johnson and West, 1973 Hartman and Shorland, 1968 Lovern, 1938 Lovern, 1938 Lovern, 1938 Lovern, 1938 West and Meng, 1968ft Tanhuanpaa and Tanhuanpaa and Moss and Lough, Moss and Lough, Moss and Lough, 2.3 5.9 26.036.2 2.2 4.9 3.8 2.87.5 3.512.5 4.2 2.1 Source 4.3 1.8 Pulliainen, 1969 Pulliainen, 1969 1968 1968 1968 n i JO Moss and Lough, 1968 i Palokangas and Vihko, 1972 03 r West and Meng, 1968a Barnett, 1970 Blem, 1973 Bower and Helms, 1969 Morton and Liebmann, 1974 "Not including 20:5 (2.1%), 22:1 (5.0%) and 23:1 (2.8%). b Range of values determined over four seasons, not including 20:0 (1.0-4.0%). c Not including 17:0 (willow ptarmigan, 2.2%; rock ptarmigan, 2.3%). d Capercaillie values include a range of four analyses, January-March. e Winter-acclimatized (W) and summer-acclimatized (S) birds. ' Range of eight localities for winter-acclimatized (W) sparrows, range of three localities for summer-acclimatized (S) sparrows. LIPID STORAGE AND UTILIZATION IN BIRDS fairly well standardized and usually include Soxhlet extraction using petroleum ether or petroleum ether and a second solvent. Analysis of samples by gas-liquid chromatography involves preparation of methyl esters of the component fatty acids which are then identified by comparison with known standards. Few scientists studying avian fat composition have been careful to separate triglycerides from phospholipids. This has probably not affected results, as many investigators have excised pieces of depot fat which usually contain little lipid other than triglyceride (Johnston, 1973), and there seems to be little difference in the composition of depot fats compared to analyses of whole carcasses TABI.E 2. Species a (West and Meng, 19686; Johnson and West, 1973). Lipids in all birds tested so far are comprised mainly of 16- or 18-carbon acids. In some cases these molecules form more than 90% of the total (Tables 1 and 2). The majority of fatty acids in most species are unsaturated. Geographic or taxonomic trends in the degree of saturation are generally not apparent. There does not seem to be a consistent compositional pattern that distinguishes migrating birds from nonmigrants, except that the 18:1/18:2 ratio tends to be greater than one in migrants and less than one in nonmigrants. Some authors have found that strongly migratory species have greater proportions of unsatu- Majorfatty acids in birds during the premigratory period or migration. 12:0 16:0 16:1 18:0 18:1 18:2 18:3 Source 10.0 17.6 7.0 5.2 28.0 20.9 11.0 33.4 1.8 3.7 Walker, 1964 Caldwell, 1973 19.3 30.2 22.4 12.0 21.7 19.9 6.3 8.4 4.7 5.0 5.7 9.2 5.8 3.6 3.5 45.3 53.2 34.1 17.0 38.5 41.8 14.9 2.2 2.6 22.8 11.0 18.1 19.8 17.9 22.4 8.3 6.0 7.8 6.4 8.1 8.1 1.3 19.9 2.6 20.3 19.9 20.9 25.8 23.5 12.0 25.6 22.5 19.3 13.0 15.1 21.7 23.2 19.9 14:0 14:1 a Sora Ruby-throated" Hummingbird Starling" Gray-cheeked Thrush" Red-eyed Vireo" Red-eyed Vireoa Philadelphia Vireo" Black and White Warbler" Tennessee Warbler" Tenneessee Warblera Nashville Warbler" Yellow Warbler" Cape May Warbler" Black-throated Blue Warbler" Black-throated Green Warbler" Blackburnian Warbler" Chestnut-sided Warbler" Bay-breasted Warbler" Blackpoll Warbler" Ovenbird" Magnolia Warbler8 Northern Waterthrush" Connecticut Warbler" American Redstart" Bobolink8 Northern Oriole" Rose-breasted Grosbeak" Indigo Bunting" White-crowned Sparrow 673 1.0 1.3 1.0 2.3 5.8 3.0 2.2 19.9 2.0 4.5 3.1 1.2 27.4 2.2 3.6 3.6 1.0 1.4 1.9 1.5 2.8 2.6 7.5 3.9 2.1 21.6 1.7 21.0 2.6 2.5 3.2 19.5 13.9 14.7 16.6 7.8 12.4 2.6 5.1 2.7 4.4 37.4 18.0 31.0 40.5 27.8 35.9 20.0 12.0 15.6 6.4 3.1 6.8 6.6 6.5 6.8 6.5 7.0 2.6 3.2 6.7 6.4 7.3 14.7 7.5 15.1 8.0 5.0 2.3 4.5 3.4 3.6 23.0 24.0 5.5 4.8 2.7 26.0 2.6 9.7 6.7 9.3 14.5 9.0 8.1 Caldwell, 1973 Caldwell, 1973 Caldwell, 1973 Walker, 1964 Caldwell, 1973 Caldwell, 1973 18.6 3.8 8.0 1.7 8.0 Caldwell, 1973 Walker, 1964 Caldwell, 1973 Caldwell, 1973 Caldwell, 1973 Caldwell, 1973 37.7 18.4 12.3 Caldwell, 1973 40.9 38.2 35.8 39.1 40.1 17.0 37.6 39.4 38.2 19.0 36.0 34.3 41.0 23.9 17.3 18.1 18.0 9.3 13.0 Caldwell, 1973 Caldwell, 1973 Caldwell, 1973 Caldwell, 1973 Caldwell, 1973 Walker, 1964 Caldwell, 1973 Caldwell, 1973 Caldwell, 1973 Walker, 1964 Caldwell, 1973 Caldwell, 1973 Caldwell, 1973 Morton and Liebmann, 1974 9.1 8.7 14.4 23.0 10.5 12.2 21.3 6.4 8.8 6.0 3.7 10.7 1.9 6.0 27.3 15.8 23.5 15.4 1.1 3.8 1.9 Includes the six major fatty acids only. "Not including 10:0 (Northern Oriole, 1.4%; Rose-breasted Grosbeak, 5.9%), 20:4 (Ruby-throated Hummingbird, 10.6%), 22:0 (Starling, 1.9%) and 22:4 (Ruby-throated Hummingbird, 4.5%). 674 CHARLES R. BLEM rated acids (Nakamura, 1963, 1964; West and Meng, 1968a; Johnston, 1973). The increased mobility of more highly unsaturated fat stores may be of adaptive significance during the metabolic demands of migration (Johnston, 1973). Hicks (1967) found the proportion of unsaturated fatty acids decreased in the Wood Thrush, Hylocichla mustelina, and Veery, Catharus fuscescens, during triglyceride deposition while the Swainson's Thrush, Catharus ustulata, showed the opposite trend. McGreal and Farner (1956) found no change in lipid composition of the White-crowned Sparrow, Zonotrkhia leucophrys, throughout the premigratory period. I have calculated iodine numbers (an index of saturation) for a variety of migratory and nonmigratory species and am unable to detect any trend in saturation (Blem, unpublished). Further studies of the triglyceride composition of depot fats of several species before and after migration are needed to clarify this problem. Seasonal variations in fatty acid composition have been discovered repeatedly (Moss and Lough, 1968; West and Meng, 1968a, b; Bower and Helms, 1969; Barnett, 1970; Palokangas and Vihko, 1972; Blem, 1973; Morton and Liebmann, 1974), and often have been ascribed to shifts in diet as have variations among species (Lovern, 1938; Walker, 1964; TanhuanpaaandPulliainen, 1969; Caldwell, 1973). Experimental tests have confirmed the importance of the composition of the diet upon depot fat composition in birds (Donaldson, 1968; Morton and Liebmann, 1974; Johnston, 1973; Edwards etal., 1973), although West and Meng (1968a) found little variation in the body composition of Redpolls, Acanthis flammea, maintained on three different diets under constant conditions. Likewise, Hazelwood (1972) concludes that variation in dietary fat has little apparent effect upon the triglyceride composition of depot fat in most birds. However, some fatty acids seem to be preferentially retained by certain species (West and Meng, 1968a; Morton and Liebmann, 1974). Christie and Moore (1972) found thatlipid composition of eggs of 23 species of birds was similar and attributed slight variations in relative abun- dance of fatty acid to dietary differences. Other factors that may affect fat composition are temperature (Fisher et al., 1962; Zar, 1967), bacterial flora in cecal fermentation (McBee and West, 1969; West and Meng, 19686; Gasaway, 1967a,b), and species differences in fat absorption and retention (Caldwell, 1973). Blem (1973), working with House Sparrows collected in midwinter at eight widely separated North American localities, found a significant negative correlation of palmitic (16:0) and positive correlation of oleic (18:1) acid levels with mean January temperatures of the collection sites. The effects of interlocality variations in diet upon geographic variation in fatty acid composition of the sparrows remain to be determined. In order to evaluate the relative importance of environmental conditions, the physiological state of the bird, and diet upon avian fat composition, further studies should be made under natural conditions. These might include analyses of a migratory species over-wintering on a monotonous diet (e.g., the Yellow-rumped warbler, Dendroica coronata, in coastal stands of wax-myrtle; see Yarbrough and Johnston, 1965), or races of the same species simultaneously studied at separate parts of the range. Food composition needs to be carefully analyzed in either case. In addition there seems to be a paucity of data on triglyceride content of forms such as the caprimulgiforms, swifts, or owls. Likewise, no comparisons of the lipid composition of closely related species maintained on the same diet have been made so as to determine phylogenetic variations in lipid deposition. QUANTIFICATION OF AVIAN LIPID Fat content of whole birds is usually determined by extracting the bird in a suitable fat solvent. Many studies have included Soxhlet extraction with a 5:1 mixture of petroleum etherxhloroform. Most extraction processes begin by drying the bird in a vacuum oven or freeze-drier. High temperatures which might alter lipid composition or drive off volatile compounds are thus avoided. The dried carcass is ground LIPID STORAGE AND UTILIZATION IN BIRDS and then extracted for one or more days and redried. The dry weight of the bird minus the lean dry weight equals the weight of fat. Fat and water content have been expressed as indices calculated as: g/100 g fresh weight, g/g dry weight, g/g fat-free weight and g/g lean dry weight. The latter is more satisfactory in some instances, since lean dry weight is a more accurate indicator of metabolic rate than fresh weight, tends to be remarkably stable within birds of the same species, sex and age (Connell et al., 1960; Rogers and Odum, 1964), and is a useful index for comparing species of different size. There is considerable variation among authors in the use of indices. Research reports should include fresh weights, lean dry weights and absolute fat content so that water and lipid indices of all types might be calculated by the interested reader. ANATOMY AND CYTOLOGY OF AVIAN FAT DEPOTS It has long been recognized (McCabe, 1943) that birds accumulate fat at specific anatomical sites in a fairly precise order. McGreal and Farner (1956) recognized 15 separate regions where fat bodies occur in the White-crowned Sparrow. Subcutaneous layers associated with the feather tracts appear in the first stages of fat deposition. Subsequent fattening results in greater amounts of subcutaneous fat, particularly in the furcular region (claviculocoracoid fat organ). In the fattest birds, subcutaneous deposits are composed of extensive masses of fat; the interfurcular region and the abdominal cavity are filled with fat. Most regions of the body show some increases in lipid content except the heart (Odum and Perkinson, 1951). King (1967) found that mesenteric adipose tissue contained relatively more fat than the subcutaneous claviculocoracoid fat organ. There seems to be no information on differences in the fatty acid composition of the lipids deposited at each site, even though one might expect variations in saturation and therefore ease in mobilization. Evidence accumulated from several species (ConneH et al., 1960; Odum et al., 1964; Rogers and Odum, 1964; Odum, 675 1965; King and Farner, 1965; Hicks, 1967; Helms etal, 1967; Johnston, 1973) indicate that avian fat bodies, unlike those of some mammals, increase in lipid content without corresponding changes in fat-free dry weight or relative water content of the body (but see King, 1967). That is, fat seems to be added toadipocyte vacuoles without an increase in adipocyte number. In addition the adipocytes apparently do not synthesize significant amounts of fatty acids but obtain fatty acid from plasma triglycerides (Goodridge and Ball, 1967; Leveille et al., 1968). Birds do not seem to possess brown fat (Johnston, 1971). Histological studies indicate no increase in adipocyte number but a considerable increase in cell volume during fattening (Hicks, 1967; Johnston, 1973). King (1967) noted an increase in water content of adipose tissue in experimentally induced fat deposition in White-crowned Sparrows, but hypothesizes that water use in migration might draw down this reserve, thus creating an apparent balance. This use of the adipocytes as a fuel "tank," coupled with the direct assembly of triglycerides from dietary fatty acids (see Ganguly et al., 1972), and the high energy yield of /3-oxidation of fatty acids, make the storage and utilization of lipids in birds a highly efficient system for storing energy. In addition, Farner et al. (1961) found that glycogen content of pectoral muscles and liver decreased and fat content increased during vernal premigratory fat deposition in the White-crowned Sparrow, but no such changes occur in the nonmigratory House Sparrow. Variations in lipid stores in pectoral muscles and other lines of evidence (George and Berger, 1966) support the idea that fat is utilized directly after conversion to fatty acids as the major fuel for sustained muscular activity in birds. FAT STORAGE AND UTILIZATION At least three strategic types of fat storage may be recognized in birds: (1) daily and seasonal cycles in fat storage of nonmigrating birds, (2) fat deposition in preparation for migration and (3) fat storage during reproduction and development. 676 CHARLES R. BLEM Daily and seasonal cycles in nonmigrants WHITE-CROWNED SPARROW Little information is available on daily cycles of fat reserves in wild birds, although many studies of body weight variations have been made. Since overnight depletion 10 of caloric reserves should be reflected in the relative obesity of birds, most information on daily adaptation comes from studies of seasonal cycles of energetics and lipid com- 9 15 3 io position. Winter fattening (Fig. 1) is a common phenonenon in small birds of the temperate zone (see King and Farner, 1966; King, FIG. 1. Seasonal fat cycles in three species of birds. 1972) and may be one aspect of "lean- The curve for White-crowned Sparrows is redrawn season" storage found in some species in from King and Farner (1965), the House Sparrow is from data in Barnett (1970) and Blem (1973) tropical habitats (Ward, 1964<z. In some curve and the Yellow-vented Bulbul curve is from data in species the level of lipid reserve may be Ward (1969). The White-crowned Sparrow is a tempinversely correlated in a proximate manner erate zone intracontinental migrant, the House Sparwith variation in ambient temperature row is a temperate zone nonmigrant and the Yellow(Odum, 1949; Odum and Perkinson, 1951; vented Bulbul a tropical nonmigrant. Helms, 1968), while these correlations are ture, than between nighttime fat reserves not detectable in other species (King, 1972). and temperatures of the day of capture or Kendeigh et al. (1969) found that weight the day before capture. This indicates that (fat) increase during the daytime in House temperature is an ultimate factor as well as Sparrows was related to either or both: (1) a proximate factor affecting winter fattenamountof weightlost duringthe preceding ing in small birds. night, (2) temperature during the daytime. Winter fat storage of small birds is selEvans (19696) found higher correlations dom extensive enough to permit survival between nighttime fat reserves of Yellow for more than overnight plus part of the Buntings, Emberiza citrinella, and the 20- following day (Table 3; also see King, year mean temperature of the day of cap- 1972). Feeding activities may begin earlier HOUSE SPARROW 111 f: YELLOW-VENTED BULBUL JAN FEB MAR APR MAY JUNE JULY AUG SEPT OCT NOV DEC TABLE 3. Overnight midwinter energetics of several species of birds. Weight Species Black-capped Chickadee1" Tree Sparrow" Bullfinch0 House Sparrowd Yellow Buntinge Dickcissel' Starling8 Willow Ptarmigan11 a (1) (2) (3) (g) Depot fat (kcal) 12.0 20.4 24.8 27.1 31.0 33.5 29.2 30.6 91.0 620.0 7.2 6.9 23.3 11.3 18.4 28.6 . 36.5 22.3 27.9 108.9 103.6 19.3 Overnight energy requirement (kcal) 8.2 10.2 15.1 22.2 17.4 6.8 31.7 99.0 Chaplin, 1974; overnight energy requirement is reduced by partial hypothermia. Calculated from Helms and Smythe, 1969 and West, 1960. Newton, 1969. d Calculated from Blem, 1973; for (1) Florida, (2) Illinois and (3) Saskatchewan sparrows. e Calculated from Evans, 19696. ' ' Calculated from Zimmermann, 19656, c. ' Blem, unpublished. h Calculated from West, 1968; West and Meng, 19686; 78.8-157.7 kcal is available for use from crop contents in midwinter (Irving ej a/., 1967). b c LIPID STORAGE AND UTILIZATION IN BIRDS and continue until dusk at times of cold stress (Beer, 1961). High fat levels in Starlings, Sturnus uulgaris, are an apparent exception and possibly reflect energy savings in the modified microclimate around man-made structures (Blem, unpublished). Winter fat storage is much below maximum capacity for storage as indicated by extremely high premigratory levels in some species (Table 4) and may indicate that extensive loads of fat and food late in each daily cycle may place small birds at a selective disadvantage not offset by the benefits of the extra energy (see Blem, 1975a). Lipid cycles in tropical nonmigrants may be of lower amplitude than those of temperate zone nonmigrants (Fig. 1). Grant (1965) found that several species of passerine birds on the Tres Maria Islands, Mexico, are fatter than mainland counterparts at the outset of the breeding season. He theorizes that the fatness supplies energy 677 and water needs for unfavorable times of the year. However, relaxed predation pressure on these islands also may permit increased loading of fat that would place the same bird at a selective disadvantage on the mainland. The magnitude of lipid storage is also partly a function of overnight energy expenditure which alternative strategies for saving or storing energy may modify. Energy may be saved by roosting in sheltered sites (Kendeigh, 1961), by huddling (see Calder and King, 1974, p. 383), partial hypothermia (as in the Black-capped Chickadee,Parus atricapillus, see Table 3) or torpidity (see Dawson and Hudson, 1970; pp. 287-297). Larger birds may supplement energy demands from food stored in the crop (e.g., Willow Ptarmigan, Lagopiis lagopus; see Table 3). Increased insulation provided by extensive subcutaneous fat deposits and/or metabolic adaptation may TABLE 4. Lipid indices (g hpidig lean dry weight) in selected species of birds. In migration Species Spring Autumn Migration Source 0.23-0.53 0.18 0.28 0.35 0.22-0.57 0.18-0.38 0.06-0.16 0.43 9 14 14 4 Permanent residents Black-necked Stilt Mockingbird Brown Thrasher Carolina Wren House Sparrow Yellow Bunting Bullfinch Cardinal 1,2, 14 5 10 14 Short-range migrants Mourning Dove Savannah Sparrow Tree Sparrow White-throated Sparrow Dark-eyed J unco 0.34 0.77 0.20 0.20-0.68 0.41-0.44 0.31 0.33 0.17-0.43 3 12 6 4, 11, 12 0.27-0.61 7 Long-range migrants Ruby-throated Hummingbird Least Sandpiper Arctic Tern Red-eyed Vireo Ovenbird American Redstart Scarlet Tanager Bobolink Dickcissel 3.13 0.25 0.30 0.54-0.67 0.45 0.34-0.43 0.87-0.97 References: 1 Barnett, 1970; 2 Blem, 1973; 3 Brisbin, 1968; 4 Caldwellrta/., 1963; 5 Evans, 1969a; 6 Helms and Smythe, 1969; 7 Helms et al., 1967; 8 Johnston, 1964; 9 McNeil, 1971; 10 Newton, 1969; H 0.74-1.39 0.86-1.51 0.73-1.29 1.17-2.16 2.13 0.37-0.53 12 15 8 4, 11, 13 4, 13 4 0.22 0.12-0.66 4, 12, 13, 14 4, 11 16 Odum, 1960a; 12 Odum, 19604; 13 Odum and Connell, 1956; 14 Odum e( al., 1965; 15 Yarbrough, 1970; 16Zimmermann, 1965A. 678 CHARLES R. BLEM also reduce energy expenditures (Blem, 1974; Kendeigh and Blem, 1974), although Newton (1969) did not believe that fattening increased insulation in the Bullfinch, Pyrrhula pyrrhula. Geographic variation in winter fattening of small birds is similar to seasonal variations in that birds in northern, colder parts of the range tend to deposit greater amounts of fat (Dolnik, 1967; Blem, 1973; see Fig. 2). Furthermore, within a single species the extent of fat deposition in geographic adaptation over the entire range may be greater than that of seasonal adjustments at a single site (see Barnett, 1970; Blem, 1973). Little work has been done on fat storage in preparation for the energetic demands of reproduction or molt. Brisbin (1969) found no significant changes in the fat content of captive Ring Doves, Streptopelia risoria, throughout the reproductive cycle. Morton et al. (1973) noted that female White-crowned Sparrows in California expend their fat reserves in caring for fledglings. Neither Newton (1968), working with 0 60 El 0 50 [1 040 £ 030 f! il 0 20 010 30 35 40 45 50 55 °N LATITUDE FIG. 2. Latitudinal variation in evening lipid reserves in House Sparrows collected in midwinter at eight sites in North America. The horizontal line is the mean, the open rectangle is one standard error above and below the mean and the vertical line is the range. The northernmost sample was collected at the northern extreme of the species' range in North America (Churchill, Manitoba), where it survives overwinter in grain storage buildings (from Blem, 1973). Bullfinches, nor Evans (19696), in a study of Yellow Buntings, found significant effects of molt upon fat levels. Migratory fat deposition Annual fat cycles in temperate zone migrants include two peaks of lipid deposition (Fig. 1). In the vernal and autumnal premigratory periods a new "set" level of obesity is established above the regular daily levels (King and Farner, 1965). At this time hyperphagia results in hyperlipogenesis that may produce extreme fatness in a few days (King and Farner, 1956; Odum, 19606; Farner, 1960; King and Farner, 1965), although Merkel (1958) did not feel hyperphagia accounted for autumnal fat deposition in the European Robin, Erithacus rubecula, or Whitethroat, Sylvia communis. During hyperphagia, metabolized energy (ingested energy minus fecal energy) levels in Whitecrowned Sparrows may increase by approximately 20% (King, 1961) and by 25-30% in Bobolinks, Dolichonyx oryzivorus (Gifford and Odum, 1965). There is no decrease in standard metabolic rate during the premigratory period (Wallgren, 1954; Merkel, 1958; King, 1961) and no apparent increase in digestive or assimilation efficiency (King, 1961; Gifford and Odum, 1965), although Zimmerman (1965a) found a slight increase in digestive efficiency that I feel is equivocal. Generally, one would expect a decrease in efficiency because greater quantities of food are being processed (Brody, 1945). Also, there seems to be no decrease in daily locomotor activity that would provide an energy savings (Farner et al., 1954; Weise, 1956; King and Farner, 1963). Morton (1967) found that wild White-crowned Sparrows fed more intensively in the middle of the day in the period just before migration and probably accumulated the surplus energy as lipid reserve. There is little evidence for adaptive shifts in food selection in the premigratory period, even though high fat diets can increase the efficiency of fat deposition in House Sparrows (Blem, unpublished). Odum and Major (1956) found that lipid levels of the diet had little effect upon the LIPID STORAGE AND UTILIZATION IN BIRDS rate of final level of fat deposition in caged White-throated Sparrows, Zonotrichia albicollis, maintained under stimulatory photoperiods. In general, it appears that premigratory fat deposition may be attributed to the extra energy intake in hyperphagia alone. The energetic costs of fat deposition or the energy produced during fat utilization have not been directly quantified although Kendeigh^a/. (1969) measured thecosts of daytime weight gains (6 kcal/g live weight) and nighttime losses (3.9 kcal/g) in House Sparrows. King (1961) used a value of 7.0 kcal/g as an estimate of the caloric equivalent of weight change in White-crowned Sparrows. Others assume that the energy equivalent of fat is 8.2-9.5 kcal/g (Odum et al., 1965; Rogers and Odum, 1964; Johnston, 1970), but since weight changes involve some water and non-fat dry materials, the difficulty of relating these values to changes in live weight remains. In White-crowned Sparrows the temporal precision of the initiation of fattening is impressive (King and Farner, 1959) and varies only a few days from year to year. In many species, premigratory deposition is rapid, but slows and finally stops as the set level is reached. Zugunruhe or nightly unrest is independent of lipogenesis and occurs even if fattening is prevented (Lofts et al., 1963; King and Farner, 1963). If the bird is starved and refed, it quickly regains the fat deposits of the original premigratory level. Kendeigh et al. (1960, 1969) theorizes that birds tend to overcompensate in storing reserves of fat when exposed to any energetic stress, including Zugunruhe. Fattening of some tropical migrants is similar to that of temperate zone migrants (Ward, 1963, 19646; McNeil and de Itriago, 1968). At least four patterns of premigratory fat deposition have been recognized: (1) short-range intracontinental migrants that begin migration before peak fatdeposition, (2) short-range intracontinental migrants that begin migration after peak deposition, (3) medium or long-range intracontinental (at least partly) migrants that begin migration before peak fat deposition and (4) long-range migrants that achieve an ex- 679 tremely high fat level before a flight over a barrier such as desert or ocean (Odum, 1960a; Odum etal., 1961; Johnston, 1964). Helms and Smythe (1969) recognize only intracontinental migrants that migrate at speeds and over distances directly correlated with fat reserves and intercontinental migrants that are similar to the former over land, but accumulate large lipid reserves as they approach barriers such as oceans and deserts (Table 4; Caldwell et al., 1963). Birds that migrate slowly and forage as they go, may not need to accumulate large lipid reserves, thus avoiding severe wing-loading problems. Fat birds tend to travel more rapidly in migration, partly because of reduced time on the ground in search of food, but also because of aerodynamic considerations (Pennycuick, 1969). Pennycuick's analysis, based upon general mechanical principles, demonstrates that adding extra weight as in premigratory fat deposition increases the power needed to fly, and also results in an increased range of flight at a higher speed. White-crowned Sparrows have greater energy reserves and a more rapid migration in spring than in autumn (King, 1963; King et al., 1963). Selection may have favored the more rapid vernal migration rate since it provides for the earliest possible arrival on the breeding grounds. Two possible limitations of migratory flight distance are fuel levels and dehydration. Extensive literature has accumulated concerning the former and it has been abundantly demonstrated that lipid levels sufficient for long-range flights are deposited (Odum and Connell, 1956; Odum et al., 1961; Odum, 1965). Flying birds lose water through evaporation from respiratory surfaces and skin and in feces and urine (Berger and Hart, 1974). The rate of loss is a function of ambient temperature and the water content of the surrounding air. At low temperatures metabolic water may be sufficient to balance water loss, but at higher temperatures loss usually exceeds production of metabolic water (Yapp, 1956; Berger and Hart, 1974). Dehydration does not seem to be critical in flights across the Gulf of Mexico (Odum et al., 1964; Johnston, 1968; Child, 1969), but 680 CHARLES R. BLEM Fogden (1972) and others have obtained evidence of dehydration in trans-Mediterranean migrants. The difference in these findings may result from variations in xIxl the environmental conditions of the mi- Q gratory flights of the birds studied. 0C Id Fat storage and utilization in eggs and nestlings The eggs of precocial birds contain more yolk than eggs of altricial birds and more yolk is retained for a longer period in precocial young (Romanoff and Romanoff, 1949; Heinroth and Heinroth, 1958; Schmekel, 1960; Ricklefs, 1974). Since 99% of the egg lipid is in the yolk, this implies an adaptive strategy of fat deposition, in which increased energy reserves support the longer incubation period and earlier selfsufficiency of precocial birds. The few available data on lipid content of eggs (Ricklefs, 1974) support this notion. After hatching, fat reserves increase throughout development of the young of both altricial and precocial species (Brenner, 1964; Ricklefs, 1967; Myrcha and Pinowski, 1969; Diehl etal., 1972; Brisbin, 1969; Brisbin and Tally, 1973). Losses of weight before or at fledging (Ricklefs, 1968) may represent the loss of some of this fat (Ricklefs, 1974; Blem, 19756) and may be the result of decreased feeding by the adults coupled with high maintenance and growth costs. Decreased water content of nestlings in later development (Fig. 3) also may account for part of the weight recession (Ricklefs, 1968; Myrcha et al., 1973; Blem, 19756). Large amounts of fat may allow young to survive periods in which adults are unable to obtain food, but for the reasons stated above, the stores may disappear before fledging, as in swifts and some seabirds (Lack, 1968). There seems to be reduced parental care in species that fledge with considerable lipid deposits (Ricklefs, 1974). Studies of parental care in conjunction with the development and composition of the young should provide much interesting information. SUMMARY This brief review has barely surveyed • . 00 1 M •i ! 50 I : Hii s f : ~ 5 1 1 1 1 * 1 1 i 1i i i • i i i < i . * . o : ' :• 10 X 08 • LLJ Q 0.6 - Q Q. 04 : 02 '. ° r • i i 2 i i 4 i i ii 6 8 10 12 14 16 AGE (DAYS) FIG. 3. Lipid and water indices (g/g lean dry weight) in nestlings of the House Sparrow from hatching to fleding. Solid circles represent individuals taken from nests, hollow circles are for laboratory-raised individuals (from Blem, 19756). some of the major features of avian strategies of lipid storage and utilization. For more detailed discussions of avian fattening, see King (1972) for a review of periodic fat storage, Berger and Hart (1974) and Berthold (1975), for a review of control, energetics and metabolic physiology of migration, and Ricklefs' (1974) survey of reproductive aspects of lipid storage and utilization. Lipid storage and utilization by birds has been extensively studied and a very large body of literature now exists on the subject. However, relatively little is known about daily and premigratory fattening in nonpasserines and most large birds, diet and the composition of depot fats in the majority of birds, the interaction and use of fat and water during migration, and variations in composition and mobility of fats deposited at different sites in the body. Birds will continue to provide much research material for students of lipids and energetic strategies. LIPID STORAGE AND UTILIZATION IN BIRDS REFERENCES 681 Fat-free weights of birds. Auk 77:1-9. Dawson, W. R. and J. W. Hudson. 1970. Birds. In G. C. Whittow (ed.), Comparative physiology of thermoregula- Barnett, L. B. 1970. Seasonal changes in temperature tion. Vol. I, Invertebrates and nonmammahan verteacclimatization of the House Sparrow, Passer domesbrates, pp. 223-310. Academic Press, New York. ticus. Comp. Biochem. Physiol. 33:559-578. Diehl, B., C. Kurowski, and A. Myrcha. 1972. Changes Beer, J. R. 1961. 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