Behavioral Ecology Vol. 12 No. 1: 22-30
© 2001 International Society for Behavioral Ecology
Influence of environmental variability on breeding effort in a long-lived seabird, the yellow-nosed albatross
a Centre National de la Recherche Scientifique, Centre d'Etudes Biologiques de Chizé (CNRS-CEBC), 79360 Villiers en Bois, France b British Antarctic Survey, Natural Environment Research Council, Madingley Road, Cambridge CB3OET, UK
Address correspondence to H. Weimerskirch. E-mail: henriw{at}cebc.cnrs.fr .
Received 9 September 1999; revised 1 February 2000; accepted 14 April 2000.
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ABSTRACT |
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The provisioning parameters, breeding success, adult mass, and survival of yellow-nosed albatrosses were studied over 7 successive years at Amsterdam Island, southern Indian Ocean. We examined the ability of this long-lived seabird to adjust its breeding effort under different environmental conditions and the fitness consequences in terms of survival and quality of offspring produced. Provisioning rate and adult mass varied extensively between years, and the lowest and highest values were associated with sea surface temperature anomalies. When waters around the island were colder, adults were in good condition and brought large meals at short intervals, whereas warmer waters resulted in lower provisioning rates, lower adult mass, and lighter chicks at fledging. Adult survival and fledging success were not affected by sea surface temperature anomalies. Yellow-nosed albatrosses appear to be unable to adjust their breeding effort every season, and their differential breeding investment probably primarily reflects different levels of food availability. Yellow-nosed albatrosses are able to regulate their provisioning behavior according to the nutritional status of their chick only when conditions are favorable. Birds appear to invest primarily in their own future maintenance rather than in provisioning. They have a wide safety margin in body mass that limits mortality risks during good years as well as during poor years. However, during unfavorable seasons adults continue to provision chicks that have a poor prospect of survival to breeding, without additional survival costs for the parents. Favorable seasons therefore have a high value in terms of fitness because of the high quality of the chick produced. We suggest that understanding how long-lived animals optimize their provisioning behavior and lifetime reproduction can only be achieved through studies encompassing several contrasted seasons.
Key words: adult mass, breeding effort, chick quality, Diomedea chlororhynchos, life history, Procellariiforms, survival, yellow-nosed albatross.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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A central issue in life-history theory is the prediction that parents should balance investment in their offspring against their own chance to reproduce in the future (Stearns, 1976
; Williams,
1966). One implication of this prediction is that long-lived
species should be less prone to trade their own survival for that of their
offspring because any reduction in adult survival would greatly reduce
lifetime reproductive success
(Charlesworth, 1980;
Goodman, 1974). It has been
suggested that, to maximize the survival of adults in long-lived species such
as seabirds, parental effort should be regulated to a fixed level of
investment, independent of the offspring needs
(Ricklefs, 1992;
Saether et al., 1993). Results
of studies on reproductive costs, especially those using an experimental
approach, are equivocal, with several studies indicating that survival costs
may occur in long-lived species (e.g., see review by
Golet et al., 1998). However,
long-lived animals such as seabirds often live in highly variable
environments, and this variability may partly explain why results on
reproductive costs are so varied, even when results of studies on the same
species are compared (Golet et al.,
1998). Because many trade-offs appear only when food is limited
(Stearns, 1992), it has been
predicted recently that high environmental variability may favor the selection
of a flexible breeding effort (Erikstad et
al., 1998). These authors predicted that during poor breeding
conditions maximum fitness is achieved by not breeding or by abandoning the
brood and that beyond a certain threshold in breeding conditions there is a
steep increase in reproductive effort but a decrease in survival. To verify
these predictions, it is necessary to study breeding effort under different
levels of resource availability.
Provisioning behavior is generally considered to be a good measure of the
breeding effort by parents. In central place foragers such as seabirds, study
of the provisioning behavior of adults reveals foraging performances at sea
and thus links foraging and life-history traits
(Nur, 1987), but also breeding
effort and environmental variability (e.g.,
Croxall et al., 1988). When
food is less available in the environment, seabirds are likely to adjust
breeding effort by modifying the rate of provisioning of the offspring
(Burger and Piatt, 1990), and
ultimately they can abandon the brood if the risk to their survival is too
great (Drent and Daan, 1980).
Conversely, years of high food availability may contribute disproportionately
to lifetime reproductive success because under this condition birds are likely
to produce offspring of good quality at low survival costs
(Erikstad et al., 1998).
Procellariiformes (albatrosses and petrels) are typical long-lived animals
sharing distinctive life-history attributes including a single-egg clutch,
slow reproductive rate, high survival, and slow chick growth (Warham,
1990,
1996). These extreme
attributes are believed to reflect the conditions of their marine environment
(Lack, 1968;
Ricklefs, 1990). However, with
their single chick, petrels and albatrosses are unable to adjust their
breeding effort by rearing more or fewer offspring. Provisioning is related to
food availability, but adults are also likely to regulate provisioning
according to the needs of the chick
(Kilner and Johnstone, 1997).
Several studies have suggested that Procellariiformes cannot modify their
provisioning behavior according to the nutritional status of their chick, but
rather they provision the chick at a fixed rate (Hamer and Hill,
1993,
1994; Ricklefs,
1987,
1992). Other studies suggest
that several species may indeed regulate provisioning
(Bolton, 1995;
Hamer and Thompson, 1997;
Weimerskirch et al., 1995,
1997,
1999). However, only one of
these studies (Weimerskirch et al.,
1999) took place over more than a single season, so knowledge is
still lacking on whether regulation abilities vary according to change in food
availability. In addition, most studies used methods based on chick weight
gains alone, which do not properly address the problem of regulation of
provisioning rates (Granadeiro et al.,
1999); therefore, monitoring individual behavior of parents is
crucial (see, e.g., Weimerskirch,
1998).
Provisioning parameters represent only investment in the chick. The body
condition of parents, rarely examined in provisioning studies, is a
fundamental parameter that cannot be dissociated from provisioning of the
offspring because it represents a degree of self-maintenance and a buffer
against the risk of increased mortality due to breeding. Adult condition also
plays a crucial role in breeding decisions
(Drent and Daan, 1980) as well
as in foraging decisions (e.g., Tveera et
al., 1998; Weimerskirch,
1998). Patterns of mass changes have been used as an index of
reproductive costs and as the outcome of adaptive compromises among different
factors (Moreno, 1989). It is
of particular interest to understand how long-lived species trade investment
in their offspring against their own body condition
(McNamara and Houston, 1996).
Most studies investigating changes over time in breeding success or
provisioning behavior have not simultaneously studied the effect of
environmental variability on adult body condition (but see
Chastel et al., 1995;
Monaghan et al., 1989).
Life-history theory would predict that in a long-lived seabird adult, body
condition should be less affected than provisioning rates by a reduction of
food availability. Investigating how adults adjust provisioning and body
condition when environmental condition and food availability vary can test
this prediction. Furthermore, no information is generally available on the
survival of adults, yet adult survival is a key parameter when measuring costs
of reproduction.
In this study we examined over several years, but also within two
contrasted seasons, the degree of variation of a series of indices of breeding
effort (individual provisioning parameters, quality of fledging, survival, and
mass of adults) in a long-lived seabird, the yellow-nosed albatross,
Diomedea chlororhynchos. This is the first time that all these
parameters have been studied simultaneously over several years in a long-lived
species. The purpose of the study was to assess the extent of variability of
these indices between seasons and within a season and thus to examine the
flexibility of breeding effort in a long-lived seabird, as well as to test the
prediction by Erikstad et al.
(1998) that under poor
environmental conditions adults should stop breeding, but that beyond a
certain threshold in breeding conditions they should increase reproductive
effort at a cost for survival.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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The study was carried out at Pointe d'Entrecasteaux, Amsterdam Island (37°50' S, 77°30' E), between January 1991 and April 1997, during the chick rearing period. Chicks hatch in early December, are left alone on the nest in late December, and fledge from the first days of April (Jouventin et al., 1983
). The
study was carried out in two adjoining colonies. One, with about 200 nests,
had been used for long-term population studies ("long-term
colony") since 1981 (see
Weimerskirch et al., 1987) and
a second, with about 120 nests, was used from 1990 onward to study the
provisioning behavior ("provisioning colony").
The study of provisioning by individual parents was carried out in 1991,
1992, 1993, 1996, and 1997. In the provisioning colony adult birds were banded
with a metal band, a plastic, colored band, and one member of the pair was
marked with a spot of picric acid on the breast to allow identification at a
distance. From mid-January to mid-February 1991, 1992, and 1993, two people
continuously observed 28-42 nests from dawn to dusk (no adult return under
darkness) to monitor the visits of the individual parent birds to the chick.
The times of arrival and departure of the adults were noted continuously,
yielding the duration of individual foraging trips. We weighed all chicks with
a 5-kg spring balance accurate to 1% at 0500 h and at 1900 h. Whenever feeding
was observed, the chick was also weighed within an hour of the departure of
the parent. No negative impact of weighing chicks frequently was noted; they
do not regurgitate food when accustomed to handling since hatching. As chicks
lose mass on the nest from respiration and defecation, the difference in mass
between the morning weighing and mass after a feed is not exactly the mass of
the feed (Ricklefs et al.,
1985). We therefore calculated the average rate of mass loss over
time according to meal size and derived a value of expected mass loss during
the time elapsed between the last weighing and the delivery of the meal. To
estimate the net mass of the meal, we added the values of expected mass loss
before the meal was delivered to the observed mass gain.
In early January 1996 and 1997, we replaced five nests with artificial
nests (Francis Scientific Instruments, Caxton, UK) incorporating an automated
system for weighing albatross chicks at 15-min intervals
(Prince and Walton, 1984).
Both the adults associated with each automated nest were fitted with a 9-g VHF
transmitter (ATS, Isanti, Minnesota, USA) taped on the back feathers. In
addition to the parents with automated nests, we fitted 12 and 20 adults
rearing chicks from 18 and 25 nests with similar VHF transmitters in 1996 and
1997, respectively. An automatic recording station, comprising a receiver, a
data logger (R4000 and DCCII, ATS, Isanti, MN) and an omni-directional antenna
were installed in a hut 200 m from the colony. The automatic recording station
continuously scanned the different frequencies. Each frequency was searched
for 10 s, so every frequency was monitored every 4-5 min. The data from the
automated nests and from the automatic receiving and recording station were
downloaded every 15-20 days using a laptop computer. The information
downloaded from the automatic recording station gives a list of frequencies,
each representing an individual for a particular time, with a number of
pulses. From these data the time of arrival and durations of the stay on land
and at sea were calculated. The simultaneous analysis of data from the
automated nest and automatic recording station permitted us to attribute each
mass increase of the chick, corresponding to a meal, to one of the two
parents. The automated nests and the logging and receiving station worked from
early January till fledging of the last chicks in mid-April. We calculated the
body condition of chicks before and after they had received a meal from the
data for growth of the chicks at automated nests. Body condition was defined
as the residual of the nonlinear regression of chick mass on time. Because
chick mass growth in Procellariiformes is complex, characterized by a period
of increase to peak mass followed by a period of mass decrease, it cannot be
described entirely by classical growth curves
(Warham, 1990). To calculate
the age and mass for the asymptote, we modeled the chick growth using
third-degree polynomial equations (SigmaPlot, SPSS Inc., Chicago). In addition
to the five chicks at automated nests, samples of 74 and 71 chicks were
weighed regularly throughout the chick-rearing period in 1996 and 1997,
respectively, and the wing length measured at the same time. In addition, on
20 March 1993 and 1995, we recorded the body mass and wing length of a sample
of chicks. We calculated the provisioning rate as the quantity of food
delivered daily to the chick by the two parents (in grams per day), hence 2
x (1/average duration of foraging trips) x meal size. To compare
values of meal size or duration of foraging trips between years, we used for
each year the period between mid-January and mid-February when information was
available every season. Although the field methodology was not the same in
1991-1993 and in 1996-1997, the duration of foraging trips is directly
comparable. For meal size, to allow comparisons between the two periods, we
used the same calculation method as described in the previous paragraph.
In the provisioning colony, between 1991 and 1997 each year, we weighed samples of adults just after they had delivered a meal during the study period of provisioning. Each individual was only weighed once a year, allowing comparison between groups through ANOVA. Some individuals may have contributed to the data set over several years, but this probably is not a serious potential source of pseudoreplication because a relatively small number of birds was sampled randomly every year in a large colony.
During a particular year or fortnight, in some cases several values of meal size and duration of foraging trips were obtained from the same individual. To account for this, for overall comparisons between years we used nested ANOVA with year as the topmost fixed level and individual birds as the nested random levels. We performed post-hoc tests using Fisher's least-significant difference (LSD) test. For comparison within season and year, we used average values for each level to avoid duplicate data for the same individual for the same categorical variables in ANOVA and Student's t tests.
We estimated annual adult survival from a group of 202 adult breeding
birds, individually marked with stainless-steel bands recaptured between 1990
and 1998 in the long-term colony (see
Weimerskirch et al., 1987, for
details of recapture procedures). The data set was first tested for
heterogeneity with Release software
(Burnham et al., 1987). The
goodness-of-fit results (test 2 and test 3) were not significant
(
202 = 29.5, p =.0791), indicating no
heterogeneity in the data set. The effect of time (t) on survival
(S) and capture rates (P), with average sea surface
temperature anomalies as a covariant were modeled using Surge 4.0
(Lebreton et al., 1992). We
selected the most parsimonious model using Akaike's Information Criterion and
tested for significance using likelihood ratio tests
(Lebreton et al., 1992).
For analysis of reproductive costs, we compared the proportions of birds
surviving to the next season for parents rearing a chick and for parents that
stopped breeding just after hatching during two successive seasons. To do
this, we searched for birds banded as breeders in the provisioning colony in
1996 and 1997 in the same colony and in the neighboring colonies
(Jouventin et al. 1983) during
the next two breeding seasons in October, just after egg laying.
The sea surface temperature (SST) anomalies were provided by IGOSS
(International Global Ocean Service System). They are estimated using monthly
SSTs blended from ship, buoy, and bias-corrected satellite data
(Reynolds and Smith, 1994). We
used average SST anomalies for January—March each season. Negative
values of SST indicate that the waters were colder than the average value
recorded since 1982. Statistical analyses were performed using SYSTAT 7.0
(Wilkinson, 1996).
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RESULTS |
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Annual variation in provisioning parameters, adult mass, and mass of fledglings
The mass of meals delivered to chicks differed between years (nested ANOVA, F4,854 = 2.98, p =.0182). In 1992 it was significantly higher than in 1991, 1993, and 1997, and in 1996 it was higher than in 1991 and 1992 (Fisher LSD post-hoc tests; Figure 1). There were significant differences between years in the duration of foraging trips (nested ANOVA, F4,1000 = 7.13, p <.0001), those in 1997 being significantly longer than in 1992, 1993, and 1996 (Figure 1). This difference was mainly the result of the occurrence of particularly long foraging trips in 1997 compared to the other years. The resulting provisioning rate varied from 227 g/day in 1997 to 392 g/day in 1992 (Figure 1).
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The mass of adults after they had delivered a meal differed between years (ANOVA, F6,384 = 6.30, p <.0001). In 1992 adult mass after meal delivery was significantly higher than any other year, and in 1997 it was lower than in any other year except 1993 (Figure 1).
The 1992 season, and to a lesser extent 1996, were characterized by high average negative SST anomalies compared to other years; waters were colder in January—March 1992 than in any other year between 1991 and 1997 around Amsterdam Island (Figure 1, Table 1). The 1991 and 1993 seasons were standard years, whereas 1997 (and 1994 and 1995) showed positive anomalies (Figure 1, Table 1). When examining the relationships between SST anomalies and provisioning parameters or adult mass, we found a significant relationship only for the duration of foraging trips and for the provisioning rate (Spearman rank correlation, rs = -.975, p <.05 and rs = -.975, p <.05, respectively; Figure 1, Table 1).
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The mass of chicks before fledging differed between years (Table 1; ANOVA, F3,308 = 11.40, p <.0001). It was lower in 1997 and higher in 1996 than in 1993 and 1994.
Annual variation in adult survival
There was no significant time dependence in the survival rates (comparison
of models St Pt and S Pt: 55 =
6.2, p >.1), indicating that there was no significant variation in
survival rates over time (Table
1). Because recapture rates were dependent on time (St Pt
compared to St P. 25 = 14.4, p
<.1), the model with time-dependent recapture rates was preferred (AIC =
1038.8). The time dependence in recapture rate was not correlated with the SST
anomalies used as covariate: Akaike's Information Criterion (1046.8) was
higher when compared to the previous model, indicating that recapture rates
were not related to SST anomalies.
Chick growth, fledging success, and return rates of adults in 1996
and 1997
The changes in mass recorded every 15 min at automated nests for one chick
in 1996 and one chick in 1997 show the typical alternation of periods of
fasting, characterized by slow mass loss, and sudden mass increases,
corresponding to the feeds delivered by adults
(Figure 2). There were
significant differences between 1996 and 1997 in growth parameters of five
chicks measured in this way each year
(Table 2). In 1996 chicks
attained a higher asymptotic mass at an earlier date, and fledged with a
higher mass, slightly but not significantly earlier than in 1997
(Table 2).
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Values for larger samples of chicks (n = 111 chicks weighed in 1996 and 80 in 1997) measured at intervals of 10-15 days confirmed that in 1996 chicks grew more rapidly, attained higher peak mass, and fledged at higher mass than in 1997, even though they were of similar mass at the end of brooding in late December (Figure 3, upper panel). There was no significant difference between 1996 and 1997 in the wing length of the chick on 20 March (ANOVA, F1,143 = 0.34, p =.5607). Fledging success was similar between the two seasons (Table 2). The return rate of adults that fledged a chick was similar to that of adults that stopped breeding (after a breeding failure) after hatching in 1996 as well as in 1997 (Table 2).
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Seasonal variation in provisioning parameters
In 1996 and 1997 there was an effect of fortnight but not of year on the
size of the meal delivered (Figure
4; two-way ANOVA, effect of fortnight, F5,88 =
4.66, p =.0008; effect of year, F1,86 = 2.68,
p =.1051; interaction, F5,86 = 1.13, p
=.3494). During both years meal size increased during the chick-rearing period
until the first fortnight of March, then declined
(Figure 4). For the duration of
foraging trips, there was an effect of fortnight and of year, with significant
interaction effects (Figure 4;
two-way ANOVA: effect of fortnight, F5,174 = 3.66,
p =.0035; effect of year, F1,174 = 12.51,
p =.0005, interaction effect, F5,174 = 8.88,
p <.0001). In 1996 the duration of foraging trips was longer in
January than in February (Figure
4) and in 1997 it was much longer during the first fortnight of
February than in the rest of the season
(Figure 4). Foraging trips were
longer in February 1997 than in February 1996 (Figures
3 and
4). As a result, the
provisioning rate in 1996 increased until the chick attained peak mass at the
end of February, than declined during March, whereas in 1997 provisioning rate
was lowest during the second fortnight of January and first of February, and
returned to similar values to those of 1996 in March
(Figure 3, lower panel).
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In 1996 and 1997 the mass of adults birds did not change significantly with the period (Figure 4; 1996, F3,63 = 1.90, p =.1383; 1997, F2,33 = 1.09, p =.3461). In the second fortnight of January adults were heavier in 1996 than in 1997 (t = 2.49, df = 27, p =.0192), whereas during the second fortnight of March there was no significant difference between the two years (t = 0.83, df = 28, p =.412).
Regulation of provisioning in 1996 and 1997
There was a tendency for meal sizes to increase with the duration of
foraging trips in 1996 (r =.1234, p =.0482, n =
260) but not in 1997 (r =.0398, p =.705, n = 93).
In 1996 the size of meal delivered was inversely related to the body condition
of chicks before they received a meal (r = -.3146, p
<.0001, n = 260), whereas there was no such relationship in 1997
(r = -.0878, p =.3007, n = 141). In 1996 the
condition of the chick after it received a meal was not significantly related
to the duration of the next foraging trip of the adult (r =.1166,
p =.6912, n = 244). Conversely, in 1997 adults leaving a
chick in good condition tended to spend more time at sea (r =.3620,
p =.0045, n = 90).
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DISCUSSION |
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Annual and seasonal variations
Interannual variability within ecosystems is a well-recognized phenomenon. It originates from cyclic or stochastic variations in oceanographic conditions due to environmental perturbations. SST anomalies have been used widely to describe ocean-ographic conditions. Although it is not well documented in subtropical waters such as around Amsterdam Island, variations in SST are known to directly affect the distribution and abundance of marine organisms such as krill, squid, or fish (e.g., Deacon, 1977
) and therefore
the distribution of top predators such as seabirds (e.g.,
Hunt, 1990) and their foraging
performance. For example, negative correlations between SST and reproductive
performance or body condition of seabirds have been found in other studies
(e.g., Guinet et al., 1998;
Springer, 1992). In this study
the negative correlation between SST anomalies and foraging performance of
yellow-nosed albatrosses suggests that SST anomalies are a good indicator of
food availability for this subtropical predator.
Seabird parameters are thought to vary nonlinearly with food availability
(i.e., to attain peak values at a certain level of food availability;
Cairns, 1987). Parameters such
as provisioning are believed to attain peaks under moderate conditions
(Cairns, 1987). The results of
our study show that foraging and provisioning parameters of yellow-nosed
albatrosses varied extensively between years. The year 1992, and to a lesser
extent 1996, appeared particularly favorable because parents were able to
perform relatively short foraging trips and at the same time to provide large
meals, and adults were much heavier than in other years. This situation
occurred when subtropical waters were abnormally cold around Amsterdam Island.
During the 1990-1993 period, the catch per unit effort of the tuna fishery
operating in the Amsterdam Island area was very high in 1992 compared to the
other years (Ardill, 1995),
suggesting that SST anomalies might represent a reasonable index of resource
availability. In contrast, the 1997 season appeared particularly unfavorable
because provisioning rate was the lowest ever recorded, and adults as well as
fledging chicks were significantly lighter than during the other seasons. The
season 1997 was characterized by the occurrence of warmer water around
Amsterdam Island. During other years when provisioning parameters were
recorded, there were no noticeable sea surface anomalies.
The environmental perturbation that occurred in 1997 was limited in duration, lasting during the second fortnight of January and the first fortnight of February only. This unfavorable episode resulted in low provisioning rates and consequently in a delay in the growth of chicks that parents were unable to compensate for when environmental conditions improved. As a result, chicks fledged with a lower mass in 1997, yet had similar wing length. This shows that low food availability can occur during only a fraction of the breeding season and can remain undetected if provisioning parameters are recorded only over a short period that does not encompass the perturbation.
These results indicate that environmental variability in subtropical waters has a profound effect on breeding effort of yellow-nosed albatrosses. Breeding effort appears particularly variable in this species in terms of provisioning parameters, but varies less in terms of adult condition, with no effect on survival.
Regulation of provisioning abilities
Considering the two components of provisioning rate, the duration of
foraging trips appears much more sensitive to change in environmental
conditions, while meal mass differs less. Similar results have been obtained
in yellow-nosed albatrosses when foraging costs are experimentally increased
(Weimerskirch et al., 2000b).
Yellow-nosed albatrosses have a specific foraging strategy in which they
forage in oceanic waters at an average distance of 350 km and do not
concentrate on a specific oceanographic sector and do not return to the same
area from one trip to the next (Weimerskirch, unpublished satellite tracking
data). They probably maximize to a great extent the mass of meals, as expected
for central place foragers (Bryant and
Turner, 1982; Cuthill and
Kacelnik, 1990; Lessels and
Stephens, 1983), and foraging success is best represented by the
duration of foraging trips.
There has been much debate about whether Procellariiformes could modify
their provisioning behavior according to the chick's needs; several studies
suggest that they are unable to do so
(Hamer and Hill, 1993;
Ricklefs 1987,
1992) and that they provision
at a fixed rate (Ricklefs and Schew,
1994). In these studies the individual behavior of adults was not
recorded, which may not allow the problem of regulation of provisioning rates
to be addressed adequately (see Granadeiro
et al., 1999). In our study the differences observed in
provisioning strategies between two contrasted seasons, 1996 and 1997, give an
indication of the way yellow-nosed albatrosses are able to adjust their
provisioning effort. When environmental conditions are favorable (1996),
parents can deliver larger meals to chicks that are in poor condition, but
this is not the case when food availability is low. This suggests an ability
to regulate provisioning according to the chick's needs, but only when
conditions are favorable. An alternative explanation is that when food
availability is high, the chick could be restrained by its swallowing
capacities, and that when it is in good condition it cannot swallow the entire
meal mass (see Hamer and Hill,
1994; Weimerskirch et al.,
1997). Conversely, during years of low food availability, chicks
could be in a chronic state of underfeeding and able to swallow the adult's
entire stomach content, which would moreover be smaller under these
environmental conditions. When environmental conditions are poor, adults
modify the duration of the foraging trips according to the condition of the
chick after it has received a meal, whereas this is not the case when
conditions are favorable. Thus, when conditions are poor at sea, adults spend
more time at sea, probably to recover some of their own body condition after
having left a chick in good condition. Yellow-nosed albatrosses spend more
time at sea when they leave the colony in poor condition
(Weimerskirch et al.,
2000b).
The results of this study indicate that, as in several other species of
petrel and albatross (Bolton,
1995; Weimerskirch et al.,
1995,
1997), the adult yellow-nosed
albatross can regulate provisioning according to the nutritional status of the
chick, but only when conditions are favorable. The contrasting results
obtained with Procellariiformes suggest that different species may differ in
their ability to regulate provisioning according to the needs of the chick,
and it has been suggested that this may arise from differences in the foraging
strategies of the species (Weimerskirch et
al., 1997). Our study indicates that the situation is even more
complex because regulatory ability not only varies between species, but that
for the same species it varies according to the environmental conditions and
the food availability encountered during the breeding season (see also
Granadeiro et al., 1998;
Weimerskirch et al., 1997,
1999). Studies investigating
regulatory abilities should therefore work at the individual level, especially
over contrasted periods of resource availability. Our study also confirms the
general idea that trade-offs appear only when food is limited
(Stearns, 1992). The
variability of provisioning rates according to food availability results in
variable chick growth and mass of chicks at fledging, whereas wing length or
fledging success did not vary between contrasted seasons.
Role of adult mass in breeding effort
There is a good concordance between changes in the mass of adults and their
rate of provisioning: adults are heavier when they provision their chick at a
high rate and lighter when provisioning rates are low. This suggests that both
the levels of self-feeding and of chick provisioning were affected by food
availability. However, adult body mass was less variable than provisioning
parameters when environmental conditions changed. During unfavorable years,
adults were only slightly lighter (4%) than during standard years, whereas the
provisioning rate was 23% lower. This reduction in body mass is likely the
result of food stress (see review in
Merkle and Barclay, 1996) due
to the lower food availability, as suggested by the simultaneous lower
provisioning rate. Birds are probably forced to tap into their reserves to
provision their chick. It is not an adaptive response to either reduce
metabolic expenditure of flight or to use the energy released by mass loss for
the chick (Norberg, 1981)
because it occurs only during the years or fortnights of low food
availability, whereas a flight adaptation hypothesis for mass loss predicts
that patterns should be same from one year to the next
(Merkle and Barclay, 1996).
The low mass reached during an unfavorable period still includes a large
amount of body reserves. Indeed, the threshold mass of yellow-nosed
albatrosses that induces the cessation of a breeding attempt
(Chaurand and Weimerskirch,
1994) is on average 1750 g
(Weimerskirch, 1999). Thus,
even during the worst period of 1997, adults were still on average 300 g
heavier than the lower threshold mass, having thus drawn only part of their
body reserves. This amount of body reserves can be considered as a
"safety margin" that is retained at the expense of provisioning
rate and indicates that birds preferentially allocate resources to the
maintenance of their own body condition at the expense of investment in the
chick.
During standard years the safety margin represents an extensive amount of
reserves—on average 23% of the threshold mass. This safety margin is
probably used to meet temporary food shortage
(Cairns, 1987), possibly to
adjust their provisioning rate (Weimerskirch,
1998,
1999), as suggested by the
temporary decline in body mass during the perturbation in 1997. Moreover, the
mass at a particular time influences the duration of the next foraging trip;
birds in poor condition spend more time foraging than birds in good condition
(Weimerskirch et al., 2000b).
When foraging costs are experimentally increased, adults also reduce their
body mass temporarily (Weimerskirch et
al., 2000b). This is what might be expected from a long-lived
species, seeking to reduce the risk incurred through increased breeding effort
when food is scarce by keeping a significant amount of body reserves, even
when conditions are unfavorable. Yellow-nosed albatrosses appear to work with
a much wider safety margin than smaller seabirds, either because they are
larger or because they are longer lived
(Weimerskirch, 1999). Although
we cannot easily separate the two effects, it is clear that it is only in
extreme circumstances that adult seabirds die because of low food availability
(Weimerskirch, 1999).
Increased mortality is more likely to be observed in species that have a
narrow safety margin (i.e., small species), and even in this case remains
limited to catastrophic situations (Vader
et al., 1990). Mortality due to low food availability is much less
likely in a large species such as an albatross.
Conversely, during the exceptionally good season when they provisioned
chicks at a very high rate, parents were 8% heavier compared to standard
years, delivered heavier meals, and their provisioning rate increased by 22%.
Specifically, adults were 31% heavier than the lower threshold mass. This
represents an extensive extra load and indicates that birds are able to carry
more mass, either as food in the stomach or as body stores, than during
standard years. This is surprising because it is generally predicted that the
amount of body reserves should be similar under conditions of medium and high
food availability and possibly lower when feeding conditions are poor
(Montevecchi, 1993). Indeed,
it is expected that birds would not accumulate additional body reserves unless
they have a functional role, mainly because the additional load could reduce
flight efficiency (Lima, 1986; see also
Cuthill and Kacelnik, 1990).
In this species the benefits of carrying extra loads of body reserves probably
outweigh the ecological costs of fat storage
(Witter and Cuthill, 1993).
Several factors may favor this, such as the lower cost of extra loads in
species using dynamic soaring flight compared to a flapping flight
(Pennycuick, 1989), as well as
the absence of predation on these larger seabirds
(Witter and Cuthill, 1993).
The benefit of extra body reserves is probably to allow this albatross to
cover foraging costs during unfavorable periods.
Fitness consequences of environmental variability
In Southern Hemisphere Procellariiformes fledging a single offspring,
breeding success is most often reduced through loss of eggs or newly hatched
chicks (Weimerskirch, unpublished data). Once chicks have been left
unattended, fledging success is generally high. In our study fledging success
was similar during the two contrasted seasons, 1996 and 1997. However, the
quality of the chick produced varied greatly from one year to the next. During
good seasons chicks are fledged with a high mass, confirming that reproduction
during good years has a large value with respect to fitness compared to bad
years (Erikstad et al., 1998).
Conversely, Erikstad et al.
(1998) predicted that during
unfavorable years maximum fitness is achieved either by not breeding or by
abandoning the brood. Yellow-nosed albatrosses still continue to invest in
their chick despite unfavorable conditions (e.g., in 1997), but they produce a
poor quality offspring at fledging. This probably has important consequences
in terms of fitness. Lower mass at fledging means a low prospect of survival
till breeding in seabirds (Magrath,
1991; Sagar and Horning,
1998; Weimerskirch et al.,
2000a). There is no evidence that changes in adult survival are
related to environmental variability, and there is no indication of a survival
cost of rearing a chick during good or poor years. This is in agreement with
the prediction that survival should not be affected by reproductive costs in
long-lived adult animals (Williams,
1966). The absence of reproductive costs due to the variable
breeding effort of the species and its extensive safety margin probably
explains why adults do not desert a chick with a low prospect of survival.
Periods of low food availability may be short or at least not last the
complete fledging period, as indicated by the 1997 season. Therefore, because
food availability may improve at any time and because adults are not at risk
themselves, they continue provisioning the chick even at low rates. However,
this contrasts with the prediction of Erikstad et al.
(1998) that birds should stop
breeding when conditions are unfavorable. Their assumptions were based on
empirical data from smaller, shorter lived seabirds such as puffins or
kittiwakes (Erikstad et al.,
1997; Jacobsen et al.,
1995). Smaller size confers a smaller safety margin
(Weimerskirch, 1999), and the
shorter life span reduces the residual reproductive value of the individuals,
making large Procellariiformes more "prudent" parents (sensu
Drent and Daan, 1980). The
available studies suggest that small species are prone to desert the chick
when conditions become unfavorable (puffins: Johnsen et al., 1994; terns:
Monaghan et al., 1992; small
petrels: Weimerskirch et al.,
1999).
In conclusion, the results of this study indicate that understanding how long-lived seabirds optimize their provisioning behavior and lifetime reproduction can only be achieved through studies encompassing several contrasted seasons. The results of previous studies investigating the problem of regulation of provisioning rates in Procellariiformes have probably been so varied and contradictory not only because they were carried out on different species of different size and different life-history traits, but also because almost all have been carried out during a single breeding season when it was not known whether individuals were under food stress or not. Understanding how seabirds optimize their breeding effort will also help predict how climatic changes will affect populations of predators in the marine environment.
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ACKNOWLEDGEMENTS |
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This study was supported by the Institut Français pour la Recherche et la Technologie Polaire (IFRTP—Program no. 109) and by the British Antarctic Survey. We thank J. Judas and P. Vallas for help with the field study in 1991-1993 and J.M. Salles in 1997, Stephen Hall for improving the English, and John Croxall, Olivier Chastel, Yves Cherel, and three anonymous referees for helpful comments on the manuscript.
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FOOTNOTES |
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P. A. Prince is now deceased.
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REFERENCES |
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