Energetics of nestling growth and parental effort in Antarctic fulmarine petrels
1 Department of Animal Science, University of California, One Shields
Avenue, Davis, CA 95616, USA
2 Australian Antarctic Division, Channel Highway, Kingston, Tasmania 7050,
Australia
* Author for correspondence at present address: Department of Biological Sciences, California State University, Long Beach, CA 90840, USA (e-mail: phodum{at}csulb.edu)
Accepted 24 March 2003
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Summary |
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Key words: doubly labeled water, reproductive effort, field metabolic rate, nestling energy budget, parental effort, Antarctic fulmarine petrel, Fulmarus glacialoides, Thalassoica antarctica, Daption capense, Pagodroma nivea
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Introduction |
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Antarctic fulmarine petrels are an excellent group in which to investigate
linkages between nestling energetics, growth rate, and parental effort. Like
other procellariiform seabirds, they exhibit a suite of life-history traits
that have long been viewed as adaptations to energy limitation arising from a
patchy and unpredictable food supply
(Ashmole, 1971)
production of a single chick, slow growth, a long juvenile period and high
adult survival (reviewed by Warham,
1990
). Yet Antarctic fulmarine petrels differ from most
procellariiform species in that their chicks can grow twice as fast as
predicted allometrically (Warham,
1990
; Hodum,
1999
). Furthermore, they breed in some of the coldest conditions
encountered by any bird, with air temperatures as low as -25°C
(Bech et al., 1988
). Relatively
fast growth in a cold environment should increase nestling energy demand and
concomitantly affect parental provisioning effort.
In this study, we used the doubly labeled water (DLW) technique to measure
adult and nestling energy requirements in four of the five fulmarine petrel
species that breed in Antarctica: the Antarctic fulmar Fulmarus
glacialoides, Antarctic petrel Thalassoica antarctica, Cape
petrel Daption capense and snow petrel Pagodroma
nivea. We combined our DLW data with information on the growth
(Hodum, 1999) and resting
energy requirement (Weathers et al.,
2000
) of nestlings to generate nestling energy budgets and examine
the assertion that petrels require considerably more energy to produce 1 g of
fledgling than other seabirds (Simons and
Whittow, 1984
). We also tested the hypotheses that nestling total
metabolizable energy requirement should be lower than predicted because of the
relatively short nestling period, but that nestling peak daily metabolizable
energy requirement should be higher than predicted because of fast growth.
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Materials and methods |
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We determined nestling and adult field metabolic rates (FMR), using the
doubly labeled water (DLW) technique
(Tatner and Bryant, 1989). We
assessed nestling FMR throughout the entire nestling period, making
measurements at 3, 9, 15, 21, 27, 33 and 39 days of age plus, for fulmars
only, 45 days of age. We determined FMR of snow petrel (N=50) and
Cape petrel (N=51) nestlings during the 199394 through
199596 seasons and Antarctic petrel (N=21) and fulmar
(N=24) nestlings during the 199596 season. We marked nests and
monitored them daily, and thus knew the exact hatch date and age of all
nestlings. No nestling was used more than once. We measured adult FMR during
the nestling provisioning period for snow (N=11) and Cape petrels
(N=26) during the 199394 through 199596 seasons and for
Antarctic petrels (N=2) during the 199596 season. We also
determined FMR for incubating snow (N=7) and Cape petrels
(N=7) during 199596.
To determine nestling FMR, we captured and weighed nestlings at the nest
and injected them intraperitoneally with 1 µl g-1 body mass of
water containing 63 atoms percent 18O and 33 atoms percent
2H. We returned nestlings to the nest for 1 h to allow the injected
material to equilibrate with body water
(Williams and Nagy, 1984) and
then removed blood samples from them (ca. 30 µl collected from a brachial
vein). 24 h later, we reweighed the nestlings and took a second blood sample.
All injected nestlings were successfully resampled over all three seasons and
all were growing normally at the time of injection. We determined natural
background isotope abundance in 46 uninjected nestlings over 23
seasons and used the mean background levels
(Table 2) in our CO2
production calculations.
|
To determine adult FMR during the nestling stage, we captured adults at the
nest after they had fed their chicks, weighed them, collected a blood sample
to establish background isotope abundance (ca. 30 µl collected from a web
vein in the foot), and then injected them intraperitoneally with 0.45 ml (Cape
petrel), 1.0 ml (snow petrel), or 1.5 ml (Antarctic petrel) of water
containing 63 atoms percent 18O and 33 atoms percent 2H.
After allowing 1 h for the injected material to equilibrate with body water
(Williams and Nagy, 1984), we
took blood samples from the birds (ca. 30 µl collected from a brachial
vein) before returning them to their nest. We recaptured adults at the nest
when they returned from their foraging trip, reweighed them, and collected a
final blood sample.
To minimize disturbance to incubation-stage adults, we used a single-sample
technique (Webster and Weathers,
1989) in which we captured each bird at the nest, weighed and
injected it, and returned it to the nest immediately. Approximately 24 h
later, we recaptured the bird, reweighed it, and collected a blood sample
before again returning it to its nest.
We stored blood samples in flame-sealed hematocrit tubes until they were
analyzed for 18O/16O and 2H/1H
ratios at the Centre for Isotope Research, University of Groningen
(Speakman et al., 1990). We
calculated rates of water efflux and CO2 production of adult
petrels from isotope turnover using the equations of Lifson and McClintock
(1966
) as modified by Nagy
(1975
), and calculated body
water volume from 18O dilution following Nagy and Costa
(1980
). Our CO2
production calculations took fractionation effects into account by assuming
that 25% of water flux represented evaporation (equation 7.17 of
Speakman, 1997
). We converted
CO2 production of both chicks and adults to energy expenditure in
kJ day-1 by assuming an energy equivalent of 26.6 J ml-1
CO2 (Ricklefs et al.,
1986
).
One perennial concern with DLW studies is whether handling alters the
animal's behavior and thus might influence its FMR. No measurable behavioral
effects were found in green-rumped parrotlets Forpus passerinus
(Siegel et al., 1999), but
substantial changes occurred in the gentoo penguin Pygoscelis papua
(Wilson and Culik, 1995
). To
evaluate whether our DLW technique affected adult petrel behavior, we compared
foraging trips of experimental birds with those of unhandled controls. All
recaptured DLW adults returned with meal sizes that did not differ from those
of control birds (t-tests: all P>0.05). Foraging trip
duration did not differ between experimental and control snow petrels
(t52=1.31, P=0.20) or Antarctic petrels
(t52=0.15, P=0.88), but experimental Cape petrels
stayed away longer than controls (2.5±0.9 versus
1.8±0.6 days, t50=3.49, P=0.01). There
was, however, no correlation between mass-specific FMR and foraging trip
duration for either Cape petrels (r24=0.23,
P=0.25) or snow petrels (r9=0.16,
P=0.63), implying that the longer trip duration of Cape petrels did
not influence their FMR.
Nestling energy budgets
We calculated nestling metabolizable energy (ME) as the sum of FMR and the
energy retained as new tissue (RE), using our empirically established linear
relationships between FMR and mass (Equations 811). We assumed ME=FMR
during mass recession, which in seabirds represents catabolism of body stores
(Roby, 1991). We employed
logistic equations for mass versus age until peak mass was reached,
and linear regression equations to describe mass once mass recession began. We
calculated nestling energy content (EC, kJ) using the following equation from
Weathers (1996
):
EC=[3.51+4.82(mM-1)]m, where m=wet mass
in g for the current day and M=adult mass. We calculated the daily
increment in retained energy (RE, kJ d-1) by subtracting the
previous day's EC value from the current day's EC. We calculated nestling
resting metabolic rate (RMR, kJ d-1) using the following
species-specific equations, derived from data of Weathers et al.
(2000
).
(syx is the standard error of the intercept;
sb is the standard error of the slope.)
Antarctic fulmar:
![]() | (1) |
Antarctic petrel:
![]() | (2) |
Cape petrel:
![]() | (3) |
snow petrel:
![]() | (4) |
Except where indicated, values are means ± 1 S.D.
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Results |
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![]() | (5) |
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Mass specific water efflux (WE, ml kg-1 d-1) was negatively correlated with body mass in nestling snow petrels and Antarctic fulmars (Fig. 2), but not in Cape petrels (r47=0.264, P=0.064) or Antarctic petrels (r19=0.252, P=0.269). The significant relationships between water efflux and nestling mass are described by the following equations.
|
Snow petrel:
![]() | (6) |
Antarctic fulmar:
![]() | (7) |
The above equations differ in slope (analysis of covariance, ANCOVA; F1,70=12.91, P<0.001), but not in intercept (ANCOVA; F1,70=0.17, P=0.68).
Nestling field metabolic rate
Nestling FMR (kJ d-1), calculated from CO2 production
as measured by doubly labeled water, increased with body mass
(Fig. 3) as follows.
|
Snow petrel:
![]() | (8) |
Cape petrel:
![]() | (9) |
Antarctic petrel:
![]() | (10) |
Antarctic fulmar:
![]() | (11) |
Although these equations differ neither in intercept (ANCOVA; F3,132=2.48, P=0.06) nor slope (ANCOVA; F3,132=2.09, P=0.10), we used the species-specific relations to estimate nestling FMR in our energy budget calculations, because errors in the TME components are additive.
Nestling mass-specific FMR (kJ g -1d-1) declined with increasing mass in snow petrels (r=0.407, N=49, P=0.003) and Antarctic petrels (r=0.483, N=21, P=0.027), but not in Cape petrels or Antarctic fulmars (Fig. 4).
|
Adult field metabolic rate and water flux
Adult Cape and snow petrels both lost significant body mass during the
incubation stage, with daily mass losses of DLW birds averaging 5.1 and 6.7%,
respectively (Table 3). These
mass losses were apparently not fully restored during the incubation recesses
when adults fed, because both Cape petrels (t31=4.43,
P<0.001) and snow petrels (t16=27.7,
P<0.001) were significantly lighter when feeding nestlings than
when incubating eggs. The mass decrease between incubation and provisioning
stages averaged 13% and 20%, respectively, for Cape and snow petrels
(Table 3).
|
Adult mass-specific field metabolic rate (ml CO2 g-1 h-1) varied between species and between the incubating and chick provisioning stages of the breeding season (ANOVA; F4,48=21.6, P<0.0001) (Table 3). Incubating adults had lower mass-specific FMR values than adults provisioning nestlings in both snow petrels (t16=6.63, P<0.001) and Cape petrels (t31=6.61, P<0.001). Mass-specific FMR did not differ between incubation stage in Cape and snow petrels (t12=1.67, P=0.12), but was significantly higher during chick provisioning in snow petrels (t35=2.01, P=0.049).
Adult water efflux rate during the chick provisioning stage was higher in snow petrels (805±157 ml kg-1d-1) than Cape petrels (634±107 ml kg-1d-1) (ANOVA; F2,36=7.48, P=0.002). Comparisons with Antarctic petrels are inappropriate, given their small sample size (N=2).
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Discussion |
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Time to fledging and fledging mass explain 9799% of the variation in
nestling TME and peak DME in 30 bird species, with increased growth rate
simultaneously yielding an increased peak DME and a decreased TME
(Weathers, 1992). Nestling
periods of Antarctic fulmarine petrels are approximately half those predicted
allometrically (Hodum, 1999
),
and thus one might expect TME values to be correspondingly reduced. Yet,
measured TME values are 3373% greater than predicted
(Table 4). Higher than expected
TME values in Antarctic fulmarine petrels, and arctic-nesting species with
relatively short nestling periods
(Weathers, 1992
), may reflect
relatively high thermoregulatory costs at high latitudes.
|
If, as suggested by Bryant and Hails
(1983), it is the peak energy
demand of nestlings that limits reproduction rather than the total or average
energy demand, one would expect interspecific variations in peak DME to
correlate with life history traits in ways that are adaptive. For example,
peak DME should be relatively low in species such as pelagic seabirds, whose
parents have difficulty obtaining food due to a widely dispersed and
unpredictable prey base (Lack,
1968
; Ricklefs,
1983
). Nestlings of the four species in this study had peak DME
values ranging from 117% (Antarctic petrel) to 166% (Cape petrel) of the
predicted values (Table 4).
These relatively high DME values reflect the rapid growth rates of fulmarine
petrels and the high costs of thermoregulation. Arctic species similarly have
higher peak DME values than predicted
(Weathers, 1996
), a result
that parallels the latitudinal gradient in hatchling metabolism
(Klaassen and Drent, 1991
).
High TME and peak DME values suggest that obtaining sufficient food is
generally not a constraint for adult fulmarine petrels, and that factors
operating at the tissue level may limit nestling growth rate in these species.
In a study of diving petrels (Pelecanoides sp.) and least auklets
(Aethia pusilla), Roby
(1991
) similarly concluded
that growth was not limited by energy intake per se, but rather by
tissue level constraints.
The relative cost of growth (Rc, TME/fledging mass) in
Antarctic fulmarine petrels is among the highest reported for birds (for a
summary, see Weathers, 1992),
with Cape petrel (71.9 kJ g-1) and snow petrel (71.7 kJ
g-1) nestlings being the most expensive to produce. These results
confirm the suggestion by Simons and Whittow
(1984
) that petrels require
considerably more energy per gram of fledgling than other species. Indeed,
including our results, the five most `expensive' fledglings to produce are all
procellariiforms, and eight of the highest nine species are seabirds
(Weathers, 1992
; and this
study). Presumably, increased thermoregulatory costs associated with a frigid
environment partly accounts for the high Rc values of
Antarctic fulmarine petrels. High Rc does not necessarily
imply a constraint on breeding birds, however. Costly fledglings may not be
disadvantageous when growth and energy requirements are dictated primarily by
developmental rather than environmental controls.
Parental energy expenditure
Nagy and Obst (1991) noted
that high-latitude seabirds that spend much time flying and/or have high wing
loading have much higher FMR values than birds generally. They found FMR
values of adults provisioning nestlings to be 200220% of the predicted
values in the least auklet, South Georgia diving petrel Pelecanoides
georgicus, common diving petrel P. urinatrix, and the southern
giant petrel Macronectes giganteus. Cape petrels and snow petrels
provisioning nestlings similarly have FMR values that average 223% and 215% of
the predicted values, respectively.
The relatively high FMR of Antarctic fulmarine petrels provisioning young
mirrors the youngs' high energy requirement, but also reflects the adults'
foraging mode, overall metabolic status and climate. Basal metabolic rates
(BMR) of adult Antarctic fulmarine petrels average 40% higher than values
predicted allometrically for nonpasserine birds
(Weathers et al., 2000). A
higher than predicted BMR, which is typical of seabirds in general and
high-latitude species in particular
(Ricklefs and Matthew, 1983
;
Ellis, 1984
;
Bennett and Harvey, 1987
;
Bryant and Furness, 1995
), is
apparently a consequence of an active lifestyle, rather than a primary
adaptation to cold (Kersten and Piersma,
1987
), and reflects the energy cost of tissues required to support
high activity levels (Daan et al.,
1990
).
Adult FMR was independent of foraging trip duration, in contrast with the
positive relationship between FMR and foraging trip duration shown by many
seabirds (Gabrielsen et al.,
1987,
1991
,
Birt-Friesen et al., 1989
;
Shaffer, 2000
; but see
Hodum et al., 1998
). We lack
data on foraging distances and at-sea activity, but if Antarctic fulmarine
petrels spend most of their time during a foraging trip in flight, then their
rate of energy expenditure would remain uniform on a daily basis. A uniform
daily rate of energy expenditure would yield an FMR that is independent of
foraging trip duration.
In addition to a high FMR, adults of all three measured species had higher
water efflux rates than predicted allometrically. Rates were 2.8 (Cape
petrel), 3.1 (snow petrel) and 3.3 (Antarctic petrel) times those predicted
for mostly aquatic birds with salt glands
(Hughes et al., 1987) and
4.35.2 times those predicted for seabirds
(Nagy and Peterson, 1988
).
Similarly high rates of water efflux were found in Cassin's auklets
Ptychoramphus aleuticus, another pelagic seabird
(Hodum et al., 1998
), and
tufted ducks Aythya fuligula (de
Leeuw, 1997
). Petrels, like auklets and tufted ducks, capture prey
at sea and thus presumably ingest water that is attached to prey items. The
high water content of these prey items may also contribute to high water
turnover rates.
Physiological work rates of parent birds can be expressed as the ratio
FMR/BMR (Drent and Daan, 1980),
a high ratio implying a high level of parental effort. Drent and Daan
(1980
) suggested that parent
birds work to their physiological capacity when rearing young and that the
FMR/BMR ratio converges on a value of 4, which denotes maximum sustainable
effort. This ratio was subsequently revised upwards to 55.7 by Weathers
and Sullivan (1989
), who noted
that relatively few species appeared to work maximally when rearing young.
Indeed, FMR/BMR ratios of breeding birds range widely from 1.36.7
(Masman et al., 1989
;
Weathers and Sullivan, 1989
;
Peterson et al., 1990
). In
seven species of high latitude (>45°) procellariiform birds other than
albatrosses, mean FMR/BMR=4.0±0.5
(Ellis and Gabrielsen, 2001
),
signifying a relatively high level of parental effort.
In both Cape and snow petrels, FMR/BMR was lower during the incubation stage, when adults were on the nest, than during the nestling stage, when they were foraging at sea (Table 3). Parental effort during the nestling period was identical in adult Cape and Antarctic petrels (3.5 times BMR), and was somewhat (but not significantly) higher in snow petrels (4.6 times BMR). These ratios are typical of other high-latitude procellariids. Thus, despite the constraints of a compressed breeding season and nestlings that grow 150200% faster than predicted, breeding Antarctic fulmarine petrels do not appear to work harder than procellariids whose chicks grow much more slowly. Presumably food is so abundant near Hop Island that adults can provision their rapidly growing chicks without additional effort.
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Acknowledgments |
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