Stomach oil, a complex mixture of neutral dietary lipids, is a unique attribute of seabirds in the order Procellariiformes. With the exception of diving-petrels, all procellariiforms produce stomach oil and feed it to their young. We conducted an interspecies cross-fostering experiment on Bird Island, South Georgia, that was designed to reveal how the presence or absence of stomach oil in meals fed to young seabirds influences their growth, development, and survival. Hatchling South Georgia Diving-Petrels (Pelecanoides georgicus), a species that lacks stomach oil, were switched with hatchling Antarctic Prions (Pachyptila desolata), a species that feeds its young stomach oil. Diving-petrel foster parents did not successfully raise prion nestlings, presumably due to the absence of stomach oil in meals fed to nestlings. Prion foster parents successfully raised diving-petrel nestlings to fledging, but growth rates were lower, nestling fat reserves were lower, and fledging was delayed compared with controls. These results suggest that stomach oil is an essential dietary component for prion nestlings to meet their energy requirements, but diving-petrel nestlings apparently cannot efficiently assimilate stomach oil. This experiment supports the hypothesis that the production of stomach oil is an adaptation that allows breeding seabirds to enhance provisioning rates of energy to the nest, while foraging on a distant and dispersed food supply. Received 21 October 1996, accepted 15 May 1997.
Alaska Cooperative Fish and Wildlife Research Unit, National Biological Service, University of Alaska,
Fairbanks, Alaska 99775, USA; and
2 Center of Marine Biotechnology, University of Maryland Biotechnology Institute, Suite 231, Columbus Center,
701 East Pratt Street, Baltimore, Maryland 21202, USA
A UNIQUE ATTRIBUTE of the breeding biology
of members of the Procellariiformes is the stor-
age of significant quantities of neutral lipids in
the proventriculus and the feeding of this
"stomach oil" to their young. Stomach oil was
once thought to be a secretory product (Mat-
thews 1949, Lewis 1966). It is now known to
have a dietary origin (Cheah and Hansen 1970,
Clarke and Prince 1976, Imber 1976, Warham et
al. 1976) and is formed by a combination of spe-
cialized gastric anatomy and physiology. The
adaptive advantage of stomach oil remains a
matter of conjecture (Warham 1977, Jacob
1982).
From the nestling's perspective, stomach oil
increases the energy density of meals and
meets the nestling's high energy requirements
for maintenance (Ricklefs et al. 1980a,b; Simons
3 Present address: Oregon Cooperative Wildlife
Research Unit, Department of Fisheries and Wildlife,
104 Nash Hall, Oregon State University, Corvallis,
Oregon 97331, USA. E-mail: robyd@ccmail.orst.edu
4 Present address: Institute of Biology, University
of Warsaw, Swierkowa 20B, P.O. Box 109, 15-950 Bia-
lystok, Poland.
and Whittow 1984). Nestling meals that con-
tain large quantities of stomach oil however,
may be deficient in other nutrients essential for
growth and may constrain growth rates (Rick-
lefs et al. 1987). It is not clear whether the lipid-
to-protein ratio of meals containing stomach oil
optimizes nestling growth and development or
whether it reflects a constraint on adult forag-
ing that imposes additional dietary constraints
on nestlings.
Diving-petrels (Pelecanoididae) are the only
procellariiforms that do not produce stomach
oil (Roby 1989, Warham 1990). Formation of
stomach oil in diving-petrels may be precluded
by the high rate of energy expenditure of adults
at sea (Roby et al. 1989, Taylor et al. 1997). Al-
though low rates of gastric emptying are essen-
tial for the formation of stomach oil they also
constrain rates of energy assimilation. Conse-
quently, formation of stomach oil may not be
feasible for species with relatively high meta-
bolic energy requirements. Also, formation of
stomach oil requires the absorption and excre-
tion of much of the salt load inherent in a zoo-
plankton meal a mechanism that poses an en-
ergetic cost of unknown magnitude (Place et al.
1989).
Cross-fostering experiments have provided
one of the most powerful tools for testing hy-
potheses on the factors constraining reproduc-
tion in seabirds. Prince and Ricketts (1981)
cross-fostered two closely related species of al-
batrosses, Black-browed Albatross (Thalassar-
che melanophris) and Grey-headed Albatross (T.
chrysostoma), which grow at different rates.
They showed that interspecific differences in
the quality of nestling diets (Clarke and Prince
1980, Prince 1980b) resulted in different
growth rates and fledging masses in fostered
nestlings compared with controls. These re-
suits indicated that the slower growth of Grey-
headed Albatrosses was at least partly a con-
sequence of lower diet quality.
Shea and Ricklefs (1985)used cross-fostering
to show that adult Gray-backed Terns (Sterna
lunata) could successfully raise chicks of the
larger Sooty Tern (S. fuscata) by increasing meal
size. They concluded that the slow growth of
Gray-backed Tern chicks was not limited by the
parents' ability to supply energy to the chick,
as suggested by Lack (1968).
We used cross-fostering to evaluate the ef-
fects of dietary stomach oil on growth and de-
velopment of seabird nestlings. Antarctic
Prions (Pachyptila desolata) and South Georgia
Diving-Petrels (Pelecanoides georgicus) were se-
lected as subjects for the experiment because
both species are small, planktivorous petrels
that nest sympatrically on some subantarctic is-
lands (Murphy and Harper 1921; Richdale
1943, 1945, 1965; Tickell 1962). These two spe-
cies are similar in size, although Antarctic
Prions (average adult body mass = 149 g; Tay-
lor et al. 1997) are somewhat larger than South
Georgia Diving-Petrels (average adult body
mass = 115 g; Roby 1989). Both species raise
only a single nestling at a time and parents re-
turn to their nest burrows to feed their young
only at night (Tickell 1962, Thoresen 1969).
Diving-petrels are thought to forage primarily
in the neritic zone (Reid et al. 1997), and both
parents normally return to the nest site with a
meal for their nestling each night (Payne and
Prince 1979, Roby 1989). Prion adults return to
the nest site less frequently (Taylor et al. 1997)
and presumably forage farther offshore. Nest-
lings of the two species are fed similar amounts
of food per day, although South Georgia Div-
ing-Petrel nestlings are fed somewhat more
biomass of food on average (43 g/day; Roby
1989) than Antarctic Prion nestlings (37 g/day;
Taylor et al., 1997). Antarctic Prions feed their
young meals that consist of about 7 to 8% stom-
ach oil by wet mass (Prince 1980a, Taylor et al.
1997). Diving-petrels do not produce stomach
oil, and young primarily are fed fresh euphau-
siids ("krill") with a lipid content of 3 to 8% of
wet mass (Payne and Prince 1979, Roby et al.
1986).
If stomach oil is an essential energy supple-
ment for prion nestlings, then those raised by
diving-petrel foster parents should exhibit
lower growth rates and delayed fledging. Al-
ternatively, if stomach oil is solely a means of
compensating for low nestling provisioning
rates, then growth and development of fostered
nestlings should not be impaired. If high di-
etary lipid-to-protein ratios or low feeding fre-
quency limits growth and development, then
prion nestlings raised by diving-petrel foster
parents should exhibit accelerated develop-
ment relative to controls. If growth rates, fat de-
position rates, and development of diving-pet-
rels are constrained by the parents' ability to
deliver energy to the nest site, then diving-pe-
trel nestlings raised by prion foster parents
should exhibit higher growth rates, larger fat
reserves, and shorter nestling periods than
controls. Alternatively, if other factors such as
essential nutrients, feeding frequency, or phys-
iological constraints limit growth in diving-
petrels, then growth of diving-petrel nestlings
raised by prion foster parents should be retard-
ed compared with controls.
The overall objective of our research was to
evaluate the significance of stomach oil for re-
production in procellariiforms. Comparisons
between control and cross-fostered nestlings of
a species that produces stomach oil and one
that does not were used to examine the rela-
tionship between stomach oil ingestion and the
growth, development, and energetics of nest-
lings.
METHODS AND MATERIALS
Field work was conducted on Bird Island (54000 ' S,
38002 ' W), located at the western end of South Geor-
gia, between 14 January and 2 April 1992. On Bird
Island, the nesting chronologies of Antarctic Prions
and South Georgia Diving-Petrels are similar, an es-
sential prerequisite for success of an interspecies
nestling-fostering experiment. Active prion and div-
ing-petrel nests were located and marked at the head
of North Valley late during the incubation period.
Nesting habitat and breeding sites of the two study
species on Bird Island are described in Payne and
Prince (1979), Croxall and Hunter (1982), and Hunter
et al. (1982).
Cross-fostering experiment.--We located and
marked 75 active nests of each species. Marked nests
were checked frequently during the hatching period;
ages of half the nestlings were known to within a
day, and ages of the remaining nestlings to within
two days. These 75 nests were assigned to either the
cross-foster or control group largely at random, al-
though we preferentially cross-fostered pairs of
hatchlings of appropriate ages (see below).
Cross-fostering was accomplished by switching
young nestlings between 30 pairs of nests as soon as
the adults had ceased brooding the nestlings during
the day. South Georgia Diving-Petrel nestlings nor-
mally are brooded continuously by their parents for
6 to 8 days posthatching, and Antarctic Prion nest-
lings are brooded continuously for only 0 to 3 days
(Ricklefs and Roby 1983). Consequently, diving-pe-
trel nestlings were cross-fostered at about 9 to 10
days posthatching with prion nestlings at about 3 to
5 days. The two species are similar in body size and
appearance at these respective ages. Switching of
nestlings occurred during the day, when both par-
ents were at sea. Previous switching experiments
with other closely related species pairs had indicated
that parents do not distinguish between their own
and cross-fostered nestlings, and that nestlings will
accept food from adults of a different species (Prince
and Ricketts 1981, Shea and Ricklefs 1985, Roby and
Lance 1994). A pilot attempt to cross-foster two pairs
of chicks of the study species on Bird Island in a pre-
vious year revealed that at least one pair of cross-fos-
tered chicks survived for an extended period under
the care of their foster parents (P. A. Prince pers.
comm.).
Growth rates of control and cross-fostered nest-
lings were monitored by weighing and measuring
known-age individuals until each nestling fledged,
disappeared, or was found dead in the nest burrow.
Nestlings were weighed every five days beginning
on day 0 (hatching day) using Pesola spring scales
(50, 100, or 300 g). We measured wing length and
fifth primary length (-+ 1 mm) beginning at day 15
for diving-petrels and day 20 for prions, the approx-
imate ages, respectively, when primaries first erupt
in the two species. We used stopped metal rulers to
measure wing length and clear plastic rulers to mea-
sure fifth-primary length. Because sample sizes of
fostered nestlings were smaller than those of con-
trols, we weighed and measured each fostered nest-
ling twice as frequently as control nestlings (i.e. at
ages 10, 12, 15, 17, 20, 22, 25, 27, etc. days posthatch-
ing).
Feeding rates of small samples of fostered diving-
petrels and fostered prions were measured on two
consecutive nights using the overnight weighing
technique (Ricklefs 1984a, Ricklefs et al. 1985) and
compared with those of control prions (Taylor et al.
1997) and control diving-petrels (Roby 1989). A de-
tailed description of the method is presented by Tay-
lor et al. (1997). Briefly, nestlings were weighed in the
evening before adults returned to the nest at night to
provision their young and at 3-h intervals thereafter
until dawn when adults returned to sea. The sum of
the positive mass increments during overnight
weighing was used as an index to the amount of food
fed to the nestling by its parents.
Volume of stomach oil in nestlings.--We measured
the volume of stomach oil (liquid lipids) in control
and cross-fostered nestlings by dilution of tritium-
labeled glycerol triether ([3H]-GTE), a nonassimila-
ble, nonmetabolizable lipid-phase marker (see Mor-
gan and Hofmann 1970; Place et al. 1989, 1991). Brief-
ly, we fed nestlings the marker in an oil carrier, and
after an equilibration period of at least 1 h we sam-
pled a small amount of the proventriculus contents
(see Taylor et al. 1997). The volume of stomach oil in
each nestling was calculated from the expression:
(Vs C/C,) - Vi, (1)
where V is the counted sample volume, V is the vol-
ume of fed marker solution, C is disintegrations/
min (DPM) in the fed solution, and Cs is the DPM in
the sample removed from the proventriculus.
Nestling fat reserves.--Fat reserves of cross-fostered
and control nestlings were estimated nondestruc-
tively using total body electrical conductivity (TO-
BEC) body-composition analysis. Nestling and
fledgling fat reserves were measured noninvasively
using an EM-Scan SA-2 Small Animal Body Com-
position Analyzer (EM-Scan Inc. 1991). Nestlings
were removed from the nest burrow during the day
when the parents were at sea, transported to the field
station where TOBEC was measured immediately
(within 1 h of removal from the nest burrow), and
returned to the nest burrow before dusk.
The TOBEC method relies on the major difference
in conductivity between lipids and other body con-
stituents to estimate total lean body mass (Pethig
1979, Van Loan and Mayclin 1987). The difference be-
tween total body mass, as determined by weighing,
and lean body mass, estimated from TOBEC, pro-
vides an estimate of total body fat. Validation studies
to date indicate that the accuracy of TOBEC-estimat-
ed lean mass can be high (r 2 = 0.996) if care is taken
to insure that subjects are: (1) properly positioned in
the chamber, (2) not hyperthermic, and (3) normally
hydrated (Bracco et al. 1983, Walsberg 1988).
Following a protocol developed by Walsberg
(1988), nestlings were immobilized by placing them
in a nylon stocking. Core body temperature of each
subject was measured (-+ 0.1øC) using a BAT-12 ther-
mocouple thermometer by inserting an esophageal
probe into the proventriculus. Subjects were then
placed on a plastic (i.e. nonconductive) carrier, se-
cured with rubber bands, and positioned in the sam-
ple chamber so that the center of the torso was in the
center of the chamber. The SA-2 was used in fixed
mode (EM-Scan Inc. 1991), and at least six replicate
TOBEC measurements were recorded for each nest-
ling. The position of each subject was changed slight-
ly several times between TOBEC measurements in
order to assure that peak TOBEC number was re-
corded. TOBEC number was calculated as the mean
of the highest measurements that were in a series of
similar values. Isolated outliers or measurements
made while the subject was moving were not includ-
ed in the analyses. This protocol was designed to
minimize error associated with variation in the po-
sition of subjects in the chamber.
Use of the TOBEC technique for estimating total
body fat of live subjects requires that a calibration
curve be developed for each species of interest (Asch
and Roby 1995). In addition, it is necessary for the
accuracy of the technique to avoid extrapolating
from calibration curves derived for adults to young
of the same species that have very different body
sizes. TOBEC calibration curves were not available
for either study species, so samples of nestlings that
were sacrificed for other objectives were used to de-
velop calibration curves. In each case, the predictive
models for total body fat were derived by regressing
total body fat (dependent variable), as determined by
proximate analysis of carcasses, against TOBEC
number and live body mass (independent variables)
in a stepwise multiple regression (Morton et al. 1991,
Skagen et al. 1993).
Following measurement of TOBEC in the live sub-
jects that were used to derive calibration curves, sub-
jects were quickly and humanely sacrificed by di-
ethyl ether inhalation. Subjects were weighed (_+ 0.01
g) on a top-loading balance, placed in plastic bags,
and frozen at -20øC for later analysis in the lab. In
the lab, subjects were partially thawed, plucked,
reweighed, and then dried to constant mass in a con-
vection drying oven at 60øC. Dried carcasses were
reweighed to determine moisture content by sub-
traction and then ground and homogenized in a
small electric meat grinder. Aliquots of dried ho-
mogenate (2 to 3 g) were extracted to determine fat
content of carcasses using a Soxtec HT-12 soxhlet ap-
paratus and petroleum ether as the solvent (Dobush
et al. 1985).
Our research followed guidelines set forth by the
Institutional Animal Care and Use Committee
(ACUC) and the American Ornithologists' Union's
Report of the Committee on Use of Wild Birds in Re-
search (Auk 105:lA-41A, 1988). The ACUC at
Southern Illinois University at Carbondale reviewed
the protocol and gave its approval.
Control Nestlings
,200
ß ' ls
I I I I I
0 10 20 30 40 50
Age (days)
FIG. 1. Growth in body mass of South Georgia
Diving-Petrel and Antarctic Prion nestlings raised in
their own nest burrows by their parents (controls)
during the 1992 breeding season at Bird Island,
South Georgia. Bars are _+ 1 SE of each age-specific
mean. See Appendix for sample sizes.
RESULTS
Growth of control nestlings.--The pattern of
growth in body mass differed between controls
of the two study species (Fig. 1; see Appendix
for age-specific body mass for control nestlings
of the two species). Antarctic Prion nestlings
grew at a higher rate, reached higher peak nest-
ling mass, had a more pronounced prefledging
mass recession, and fledged at an older age and
a greater body mass than South Georgia Div-
ing-Petrels. These differences in part are due to
the fact that prions are larger than diving-pet-
rels (mean body mass = 149 g vs. 115 g, re-
spectively). The peak nestling mass of prions
(215.9 + SD of 30.2 g at 40 days, n = 30) was,
however, greater than that of diving-petrels
(133.7 + 20.2 g at 35 days, n = 31) relative to
adult mass (145% vs. 116%, respectively). Pre-
sumably, this reflects the deposition of larger
fat reserves by prion nestlings.
Growth of cross-fostered nestlings.--Less than
half (n = 14) of cross-fostered prions (n = 30)
survived to the age of 10 days. Subsequent
mortality of the surviving cross-fostered
prions was comparatively low until about 30
days, after which their condition deteriorated.
None survived to the average fledging age of
control prions (ca. 52 days), because all had to
200
100
200
150
100
50
control
?otrol
5thprimary'" .
10 20 30 40 50
Age (days)
FIG. 2. Growth in body mass (A) and wing length
and fifth-primary length (B) of Antarctic Prion nest-
lings raised by South Georgia Diving-Petrel foster
parents (cross-fostered) compared with control
prion nestlings. Bars are _+ 1 SE. Sample sizes of
cross-fostered prion nestlings are as follows (age in
days/n): 5/24, 7/19, 10/14, 12/14, 15/13, 17/13,
20/13, 22/13, 25/12, 27/11, 30/10, 32/8.
150
100
5O
f, cross-fostered
control
100
50
5th p ' -
0 10 20 30 40
Age(days)
FIC. 3. Growth in body mass (A) and wing length
and fifth-primary length (B) of South Georgia Div-
ing-Petrel nestlings raised by Antarctic Prion foster
parents (cross-fostered) compared with control div-
ing-petrel nestlings. Bars are _+ 1 SE. Sample sizes of
cross-fostered diving-petrel nestlings are as follows
(age in days/n): 10/24, 12/29, 15/27, 17/25, 20/24,
22/24, 25/21, 27/20, 30/19, 32/18, 35/18, 37/18,
40/18, 42/17, 45/16.
be euthanized by age 40 days. Growth rate of
total body mass in cross-fostered prions was
much lower than in control prions (Fig. 2A).
Cross-fostered prions appeared to reach an as-
ymptotic body mass of about 100 g by about 20
days posthatching. The dramatic differences in
growth of body mass also were apparent in
growth of wing length and fifth primary length
(Fig. 2B). Average wing length of cross-fos-
tered prions was consistently less than that of
controls (t-values = 6.88 to 7.48 for compari-
sons at 20, 25, and 30 days posthatching; Ps <
0.00001).
In contrast, most cross-fostered diving-pet-
rels (17 of 30; 57%) survived until fledging age
(ca. 45 days), and their body mass at that age
(113.8 + 16.5 g, n = 13) was similar to that of
controls (110.8 _+ 14.5 g; t = 0.47, n = 11, P =
0.64). There were, however, differences in
growth and development between control and
cross-fostered diving-petrels (Figs. 3A, B).
Growth in body mass of fostered diving-pet-
rels lagged behind that of controls. At ages 15,
20, and 25 days, fostered diving-petrels had
significantly lower body mass than controls (P
< 0.0005 for each of three t-tests; Fig. 3A). By
age 30 days, fostered diving-petrels (124.0 +
24.3 g, n = 16) were no longer significantly
lighter than controls (132.5 + 18.0 g, n = 39; t
= 1.44, P = 0.156).
Wing length of fostered diving-petrels was
not different from controls on day 15 (P = 0.76),
day 20 (P = 0.12), or day 25 (P = 0.11) but was
significantly less than controls on day 30 (P =
0.025), day 35 (P = 0.001), day 40 (P = 0.0006),
and day 45 (P = 0.002). Although age-specific
means for wing length of fostered diving-pet-
rels were significantly less than controls late in
the nestling period, the actual differences be-
tween means were small (Fig. 3B). Finally, 94%
of surviving fostered diving-petrels (16 of 17)
fledged after age 45 days, whereas only 41% of
control diving-petrels (12 of 29) fledged after
45 days. Indeed, fostered diving-petrels
fledged at a significantly older age compared
with controls (X2c = 10.4, P = 0.0013). The later
fledging of fostered diving-petrels probably
was related to lower rates of wing growth.
We estimated the mass of food delivered per
night to fostered diving-petrels by their prion
foster parents from the sum of positive mass
increments recorded overnight at 3-h intervals
(SUM; after Ricklefs 1984a). Nine fostered div-
ing petrels were weighed overnight on two
consecutive nights (4 and 5 March) for a total
of 18 nestling nights. The average age of these
nestlings was 32 --+ 3.7 days (n = 18), close to
the age of peak nestling mass. The average
SUM for this sample of fostered diving-petrels
(22.1 --+ 15.62 g, range 0 to 45 g, n = 18) was not
significantly different from the average SUM
for control prion nestlings (31.3 + 23.4 g, n =
57), but the variance in SUM was high for both
samples, and sample size for fostered diving-
petrels was small, resulting in low power to de-
tect a difference if present. Average NET (i.e.
mass change over 24 h due to the previous
night's feeding) of fostered diving-petrels
(-1.33 -+ 17.31 g, n = 18) was not different from
0 or the average NET of control prion nestlings
(2.0 --+ 13.99 g, n = 34), but sample size for the
former was small and variance in NET was
high. The regression equation of NET on SUM
was:
NET = -11.38 + 0.511(SUM) (2)
(r 2 = 0.59, F = 18.85, df = 1 and 13, P = 0.0008,
SE of slope = 0.118).
Five cross-fostered prions also were weighed
on the same two nights; the average SUM of
this small sample was 20.7 -+ 9.46 g (range 9 to
42 g, n = 9 nestling nights). The corresponding
value for NET was -0.25 + 5.75 g (n = 8 nest-
ling nights), also not different from 0. The re-
gression equation for NET on SUM was:
NET = -9.74 + 0.444(SUM) (3)
(r 2 = 0.58, F = 8.24, df = 1 and 6, P = 0.028, SE
of slope = 0.155).
The only available SUM and NET data for
control diving-petrels were collected at the
same study site during the 1982 breeding sea-
son (Roby 1989). Growth rates of control div-
ing-petrel nestlings in 1992 (Appendix) and
1982 (D. Roby unpubl. data) were quite similar,
suggesting that average provisioning rates to
diving-petrel nestlings were similar in the two
years. The average SUM for control diving-pe-
trel nestlings in 1982 was 41.6 _ 11.4 g, and the
average NET was 0.69 - 6.7 g (n = 78 nestling
nights). Although the average value of NET
was similar between control diving-petrels and
fostered prions, the average value of SUM for
the small sample of fostered prions was only
about half that of control diving-petrels (20.7 g
vs. 41.6 g).
An analysis of covariance revealed that the
slope of the regression of NET versus SUM for
fostered diving-petrels (0.511)was significant-
ly greater (F = 6.67, df = 1 and 54, P = 0.013)
than the slope of the regression for control div-
ing-petrels (0.251; data from 1982). This sup-
ports the assumption that prion parents fed
stomach oil to fostered diving-petrel nestlings,
resulting in a higher conversion efficiency of
food to nestling body mass compared with
controls. The higher slope of NET versus SUM
for fostered diving-petrels was not an artifact
of using younger nestlings in the analysis; on
average, fostered diving-petrels in this sample
were older (32 days) than control diving-pet-
rels (25.7 - 7.37 days, n = 78).
Volume of stomach oil in nestlings.--Volume of
stomach oil was measured in control prions (n
= 44), control diving-petrels (n = 17), fostered
prions (n = 8), and fostered diving-petrels (n =
15) using the GTE dilution technique. The ex-
perimental error in this technique averaged +
3.5% (Place et al. 1991), so measured stomach-
oil volumes of <0.1 mL are not different from
zero. The distribution of stomach-oil volumes
in control prion nestlings was highly skewed,
with most individuals containing little stomach
oil and only a few storing 5 to 15 mL (Taylor et
al. 1997). Stomach-oil volume of fostered prions
(median = 0.02 mL, range 0 to 0.21 mL) was
lower than that of control prions (median =
0.87 mL, range 0 to 14.07 mL; Mann-Whitney
U = 73.5, P = 0.009). Stomach-oil volume of
fostered diving-petrels (median = 0.03 mL,
range 0 to 5.05 mL) was not different from that
of control diving-petrels (median = 0.00 mL,
range 0 to 0.17 mL; U = 93.0, P = 0.193). Three
fostered diving-petrels, however, had measur-
able volumes of stomach oil (>0.1 mL), where-
as no control diving-petrels had detectable
amounts of stomach oil. Fostered diving-pet-
rels nevertheless had significantly lower
amounts of stomach oil than did control prions
(U = 198, P = 0.021). Therefore, no nestlings
fed by diving-petrel parents had measurable
volumes of stomach oil, whereas nestlings fed
by prion parents did. Of the nestlings fed by
prion parents, few diving-petrels (20%) stored
measurable amounts of stomach oil, whereas
the majority (61%) of control prions did.
Nestling fat reserves.--We collected samples of
45-day-old control (n = 7) and fostered (n = 8)
diving-petrels to test the hypothesis that dif-
ferences in diet resulted in differences in body
composition of nestlings at the age of fledging.
Although control diving-petrel fledglings had
higher average total body mass, lean body
mass, lean dry mass, total body fat, and percent
fat of total body mass compared with fostered
diving-petrel fledglings, all differences were
small and not significant (t-tests, P -> 0.38).
Potential differences in body composition of
control and cross-fostered nestlings were fur-
ther investigated using estimates of body com-
position obtained through TOBEC analysis.
Three different TOBEC calibration curves for
predicting total body fat from TOBEC number
were developed: (1) for nestling South Georgia
Diving-Petrels near the age of peak body mass
(30 to 35 days posthatching), (2) for fledgling
South Georgia Diving-Petrels (ca. 45 days), and
(3) for nestling Antarctic Prions near the age of
peak body mass (35 to 40 days). Two indepen-
dent variables (TOBEC number and live body
mass) explained a significant proportion of the
variation in total body fat and entered the step-
wise regression used to derive each of the three
calibration curves. Subject body temperature
did not enter the regression models. The cali-
bration equation for nestling South Georgia
Diving-Petrels at the age of peak body mass
(ca. 30 days) was:
Total body fat = -35.9 + 0.725
(Live body mass)
- 0.178
(TOBEC number) (4)
(F-ratio = 23.54, df = 2 and 13, r 2 = 0.784, P <
0.0001; mean error = 13.5%, range 3.3 to
70.5%). The calibration equation for fledgling
South Georgia Diving-Petrels (ca. 45 days) was:
Total body fat = -28.2 + 0.588
(Live body mass) (5)
- 0.093
(TOBEC number)
(F-ratio = 111.1, df = 2 and 12, r 2 = 0.949, P <
0.0001; mean error = 6.9%, range 0.2 to 18.2%).
The calibration equation for nestling Antarctic
Prions at the age of peak mass (ca. 35 days)
was:
Total body fat = -41.055 + 0.949
(Live body mass) (6)
- 0.42
(TOBEC number)
(F-ratio = 69.43, df = 2 and 13, r 2 = 0.914, P <
0.0001; mean error = 7.2%, range 1.0 to 15.8%).
In all three cases, error was calculated using
the formula:
IF - PF]/F x 100, (7)
where F is total body fat (g) and PF is predicted
total body fat from the TOBEC calibration
equation.
TOBEC number and live body mass were
measured on a sample of 37 diving-petrel nest-
lings (17 control 20 fostered). The average age
of these nestlings was 31.1 -+ 1.71 days (range
26 to 36), and there was no difference between
the average age of control and fostered nest-
lings (t = 1.13, P = 0.27). There was, however,
a significant difference between the live body
mass of control nestlings (137.2 + 18.45 g) and
fostered nestlings (120.4 + 16.72 g; t = 2.91, P
= 0.0063). Total body fat was then estimated for
each nestling using the appropriate TOBEC cal-
ibration equation (equation 4). Estimated total
body fat was higher in control nestlings (29.8 +
8.80 g) than in fostered nestlings (19.25 + 8.09
g; t = 3.80, P = 0.0006). Percent body fat of live
mass was then calculated to compensate for the
difference in live body mass between the two
groups. Estimated percent body fat of control
diving-petrel nestlings (21.3 -+ 4.28%) was
higher than that of fostered diving-petrel nest-
lings (15.47 -+ 5.32%; t = 3.62, P = 0.0009).
A sample of eight 45-day-old fostered div-
ing-petrels (i.e. fledglings) was analyzed using
TOBEC, and the estimated total body fat of
these fledglings was added to those of the sam-
ple of 15 diving-petrel fledglings that were
used to derive the calibration curve (equation
5). Estimated total body fat of control diving-
petrel fledglings (22.42 __+ 5.085 g; n = 7) still
was not different from fostered fledglings
(22.97 __+ 8.798 g; t = 0.15, n = 16, P = 0.879).
Finally, we measured TOBEC number and
live body mass on a sample of 15 prion nest-
lings (11 control, 4 fostered). The average age
of these nestlings was 32.9 --+ 3.92 days (range
25 to 41 days), and there was no difference be-
tween the average age of control and fostered
nestlings (t = 1.43, P = 0.18). There was a sig-
nificant difference between the live body mass
of control nestlings (185.7 -+ 28.46 g) and fos-
tered nestlings (103.6 -+ 16.44 g; t = 5.38, P =
0.0001). Total body fat was estimated for each
nestling using the appropriate TOBEC calibra-
tion equation (equation 6). Despite small sam-
ple sizes, estimated total body fat from TOBEC
was much higher in control prion nestlings
(42.3 --+ 17.11 g) than in fostered prion nestlings
(3.71 +_ 8.36 g; t = 4.25, P = 0.0009). Also, es-
timated percent body fat of control prion nest-
lings (22.3 -+ 6.72%) was much higher than that
of fostered prion nestlings (2.6 + 8.45%; t =
4.71, P = 0.0004).
DISCUSSION
Growth of control and cross-fostered nestlings.-
The results of the cross-fostering experiment
are consistent with the hypothesis that stomach
oil provides an essential dietary energy sup-
plement for prion nestlings. Prion nestlings
that survived the first week under the care of
their diving-petrel foster parents grew poorly
and appeared to be chronically undernour-
ished. The results do not support the alterna-
tive hypotheses that growth of prion nestlings
is constrained by either the high dietary lipid-
to-protein ratio or the low frequency of meal
delivery.
The growth of fostered diving-petrels was
retarded compared with that of controls, but at
the time of fledging, body size, mass, and com-
position differed little between control and fos-
tered diving-petrels (Figs. 3A, B). These results
support the hypothesis that growth of diving-
petrel nestlings is limited by essential nutrients
(other than energy), the frequency of meal de-
livery, or physiological constraints. The alter-
native hypothesis that growth is limited by the
parents' ability to deliver energy to the nest
was not supported.
We collected some data on the provisioning
rates to fostered diving-petrel and prion nest-
lings using the overnight weighing technique,
but sample sizes were too small to rigorously
test the hypothesis that fostered nestlings were
provisioned at the same rate as their control
counterparts. Evidence suggested that some
fostered nestlings were rejected or poorly pro-
visioned by their foster parents immediately af-
ter the cross-fostering event, especially fos-
tered prion nestlings. Half of the fostered prion
nestlings were dead or in very poor condition
within a week of being moved to diving-petrel
nests. Also, the limited data available on pro-
visioning rates to fostered prion nestlings (n =
9 nestling nights) suggest that at least some of
the survivors were not fed as much food as con-
trol diving-petrels. Consequently, it is possible
that some of the differences in growth between
control and cross-fostered prion nestlings re-
sulted from abnormal nestling-feeding behav-
ior on the part of diving-petrel foster parents.
The slope of the regression of NET versus
SUM was significantly greater for cross-fos-
tered diving-petrels than for controls, indicat-
ing that the former were fed stomach oil by
their prion foster parents. Evidence suggested
that diving-petrels had difficulty with the
stomach oil that their prion parents fed them.
During periodic weighing and measuring of
fostered diving-petrels, we noticed that the
plumage of some nestlings, especially the head
and breast feathers, was soiled with stomach
oil. Growth in body mass of fostered diving-
petrels also was more erratic compared with
controls (Fig. 3A), suggesting that occasional
delivery of meals especially high in stomach
oil, and/or gaps in delivery of food by prion
foster parents, were responsible for temporary
reductions in growth rate of body mass. It
seems plausible, therefore, that fostered diving-
petrels grew more slowly than controls because
of physiological constraints in their ability to
efficiently digest and assimilate stomach oil, as
well as because feeding rates were lower. We
found no evidence in support of the alternative
hypothesis that essential nutrients other than
energy limited the growth of fostered diving-
petrels.
Nestling provisioning rates.--South Georgia
Diving-Petrel nestlings are fed on average 1.8
meals each night, usually one meal from each
parent (Roby 1989), whereas Antarctic Prion
nestlings are fed on average 1.1 meals each
night (Taylor et al. 1997). Average meal size for
diving-petrel nestlings is 23.3 g (Roby 1989),
whereas prion nestlings are fed meals that av-
erage 31.7 g (Taylor et al. 1997). Consequently,
diving-petrel nestlings raised by prion foster
parents would, on average, be fed less food per
day (ca. 17% less) than they normally receive
from their own parents. Conversely, prions
raised by diving-petrel foster parents would,
on average, be fed about 20% more biomass of
food per day then they normally receive from
their parents.
Taylor et al. (1997) estimated that prion par-
ents feed their nestlings an average of 3 mL of
stomach oil per day. This amount of stomach
oil in prion diets boosts the energy density to
about 7.6 kJ/g wet mass, compared with 5.8
kJ/g wet mass for diving-petrel diets that lack
stomach oil (Roby 1991). This means that prion
nestlings are fed about 280 kJ / day versus about
250 kJ/day for diving-petrels, a difference suf-
ficient for control prions to grow at a higher
rate and deposit larger fat reserves than control
diving-petrels. Thus, stomach oil appears to be
an essential adaptation for enhancing the en-
ergy density of nestling meals in petrel species
that feed their young less frequently than div-
ing-petrels.
Volume of stomach oil in nestlings.--Results of
the GTE dilution-space experiments support
the conclusion that adult diving-petrels do not
form stomach oil and do not feed stomach oil
to their young. The measurement of small
amounts of stomach oil (up to 5 mL) in a few
fostered diving-petrels suggests that diving-
petrels can store stomach oil in their proven-
triculus if it is a component of their diet. Taylor
et al. (1997) reported that the majority of prion
nestling meals do not contain stomach oil. This
would explain the unexpectedly low propor-
tion of control prions and fostered diving-pet-
rels with measurable amounts of stomach oil in
their proventriculi. It also may explain how
prion parents can raise foster diving-petrel
nestlings despite the latter's apparent difficulty
in digesting and assimilating stomach oil.
Nestling fat reserves.--Estimated total body
fat from TOBEC measurements indicated that
control diving-petrel nestlings at the age of
peak body mass were able to deposit signifi-
cantly larger fat reserves than fostered diving-
petrels. Similarly, control prion nestlings at the
age of peak body mass were able to deposit
much larger fat reserves than fostered prions
(most fostered prions had essentially no fat re-
serves). The difference between treatments in
the fat reserves of diving-petrel nestlings no
longer was apparent by the average fledging
age (ca. 15 days later). In the intervening peri-
od, fostered diving-petrels had deposited more
fat reserves, and control diving-petrels had me-
tabolized some of theirs. These results suggest
that diving-petrel nestlings seek to achieve a
target level of fat reserves prior to fledging.
They also suggest that fostered diving-petrels,
despite apparent difficulties in adjusting to
prion diets and feeding regimes, were able to
compensate by late in the nestling period.
Estimates of total body fat also indicated that
fat reserves of control prions at the age of peak
body mass were very similar to those of control
diving-petrels when expressed as a proportion
of total body mass (22.3% and 21.3%, respec-
tively). This suggests that prions and diving-
petrels have similar target levels for fat re-
serves, once results are adjusted for differences
in body size.
Prions may grow at a higher rate and fledge
with larger fat reserves than diving-petrels be-
cause dietary stomach oil can meet all of the
nestling's energy requirements without catab-
olizing dietary protein (Roby 1991). This is con-
sistent with the idea that the slow growth of
some pelagic seabirds is the result of con-
straints involving tradeoffs in the management
of available energy for reproduction by the par-
ent-offspring unit (Ricklefs 1984b). But it begs
the question of why diving-petrels (and other
pelagic seabirds) do not feed their young stom-
ach oils. The absence of stomach oil in diving-
petrels may be a consequence of higher nest-
ling feeding rates, higher gastric emptying
rates, inappropriate gastrointestinal anatomy,
or some combination of these factors.
Diving-petrels are pursuit-divers that ex-
pend energy at a relatively high rate while for-
aging (Roby and Ricklefs 1986) compared with
prions (Taylor et al. 1997). Taylor et al. (1997)
proposed that the high field metabolic rates of
diving-petrels preclude the formation of stom-
ach oil and the allocation of this high energy
component of the diet to their young. This, cou-
pled with high rates of meal delivery to nest-
ling diving-petrels compared with other pro-
cellariiforms, provides an explanation for the
absence of stomach oil in the diets of nestling
diving-petrels.
For petrels that forage far from the nest site,
there is a clear energetic advantage to feeding
nestlings a diet that consists largely of stomach
oil. By concentrating dietary lipids in the pro-
ventriculus, adults can reduce the mass of nest-
ling meals and the frequency of meal delivery,
thus lowering the time and energy costs of
transporting food from the foraging area to the
nest (Ashmole 1971, Laugksch and Duffy 1986,
Obst and Nagy 1993). Both breeding and non-
breeding adults store stomach oil, however,
suggesting that it is not solely an adaptation for
reproduction (Jacob 1982). Metabolism of stom-
ach oil at sea may preclude the energy cost of
synthesizing fat depots from assimilated fatty
acids and of later mobilizing those energy re-
serves from adipose tissue during fasts, costs
that amount to 25 to 30% of the assimilated en-
ergy (Ricklefs 1974, Spady et al. 1976). It is like-
ly that these same energy savings confer a ben-
efit to nestlings that store stomach oil in lieu of
body fat as an energy reserve.
ACKNOWLEDGMENTS
We thank Dr. J.P. Croxall, P. A. Prince, and British
Antarctic Survey support staff at the Bird Island Re-
search Station and the Cambridge headquarters for
their invaluable and generous assistance in making
this research possible. The initial phase of this re-
search was accomplished while the first and second
authors held positions with the Cooperative Wildlife
Research Laboratory and the Department of Zoology
at Southern Illinois University Carbondale. This re-
search was supported by National Science Founda-
tion grant DPP 90-18091 to DDR. An earlier version
of the manuscript was improved by the reviews of J.
M. Morton, T. R. Simons, and an anonymous referee.
This is Contribution No. 295 from the Center of Ma-
rine Biotechnology, University of Maryland Biotech-
nology Institute.
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Associate Editor: M. E. Murphy
APPENDIX. Age-specific body mass ( _+ SD) of
nestling South Georgia Diving-Petrels and Antarc-
tic Prions (controls only) during the 1992 breeding
season on Bird Island, South Georgia. Age is in
days posthatching.
Age Mass (g) n
South Georgia Diving-Petrel
0 15.3 _+ 2.5 52
5 32.9 -+ 5.5 47
10 50.1 _+ 10.4 44
15 79.5 -+ 11.8 43
20 105.3 _+ 15.7 42
25 120.9 +_ 18.7 39
30 132.5 ñ 18.0 39
35 133.7 _+ 20.2 31
40 128.8 _+ 18.4 30
45 110.8 _+ 14.5 11
Antarctic Prion
0 25.4 -+ 4.8 54
5 58.5 +_ 13.2 56
10 90.8 -+ 16.7 55
15 129.2 _+ 21.7 54
20 165.9 _+ 23.8 54
25 188.6 _+ 22.6 53
30 205.8 -+ 27.4 50
35 214.8 +_ 29.4 38
40 215.9 +_ 30.2 30
45 210.2 _+ 17.2 25
50 174.2 -+ 15.3 19