Download Patterns of Lipid Storage and Utilization in Birds It is axiomatic that

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
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02
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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
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681
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