Experimental Gerontology 38 (2003) 757–760
www.elsevier.com/locate/expgero
Actuarial and reproductive senescence in a long-lived seabird: preliminary
evidence
D.J. Andersona,*, V. Apaniusb
b
a
Department of Biology, Wake Forest University, Winston-Salem, NC 27109 7325, USA
Department of Biological Sciences, Florida International University, Miami, FL 33199, USA
Abstract
The evolutionary theory of aging predicts that pelagic seabirds, which have low extrinsic mortality, should show exceptional longevity.
These taxa appear to show the lowest rates of actuarial senescence among birds yet display declining reproductive performance at advanced
ages. We have studied survival and reproduction of Nazca boobies (Sula granti) in the remote Galápagos Islands since 1984. We found a
slight but detectable increase in mortality rate in the oldest ($19 yrs) cohort, indicating minimal actuarial senescence. The probability of
successful reproduction (eggs or fledglings) declined from mid-life to the age of the oldest cohort. We are currently investigating the causal
relationship between physical (foraging) performance, components of reproductive success, and longevity at our pristine study site.
q 2003 Elsevier Science Inc. All rights reserved.
Keywords: Reproduction; Actuarial senescence; Seabird; Nazca booby; Sula granti
1. Introduction
Birds and bats live longer for their body size than do
non-flying mammals, probably because flight protects them
from some sources of extrinsic mortality (Calder, 1983;
Austad and Fischer, 1991; Holmes and Austad, 1995).
Pelagic seabirds show a further enhancement in lifespan,
with greatly delayed actuarial senescence compared to other
birds (Ricklefs, 1998). Here we examine data on survival
and reproduction of wild adult Nazca boobies (Sula granti),
a pelagic seabird nesting in the Galápagos Islands, for
evidence of either actuarial or reproductive senescence,
using our long-term demographic data. This population has
been monitored since 1984 and, unlike some other seabird
populations (Nisbet, 2001), appears to show little anthropogenic effect on their biology.
2. Materials and methods
2.1. Actuarial senescence: longitudinal analysis
We have studied Nazca boobies (a recently identified
taxon; Friesen et al., 2002) at Punta Cevallos, Isla Española,
Galápagos Islands, Ecuador since 1984, focusing on
* Corresponding author. Tel.: þ 1-336-758-5319; fax: þ1-336-758-6008.
E-mail address: da@wfu.edu (D.J. Anderson).
behavioral ecology (e.g. Anderson, 1989; Anderson and
Ricklefs, 1995; Clifford and Anderson, 2001). Breeding is
seasonal, with laying from September – February, and most
fledging completed by June (Anderson, 1993). Leg-banding
of adults and young of the year began in 1985, and DJA has
conducted a band-resight survey at the beginning of each
breeding season (except the 1988 – 1989 season) each year
since the 1985– 1986 season. Details of the survey are given
by Huyvaert and Anderson (in press). Briefly, sweeps are
made through the breeding colony at night when the number
of birds present is highest and capture is easiest, and leg
bands of all adults present are recorded. Each resighted bird
receives a temporary mark to ensure sampling ‘without
replacement’. Since not all birds are present on all nights,
each area of the colony is visited on consecutive nights until
the expected number of new birds from a regression model
is less than 1. Until 1992, aluminum leg bands were used,
with an annual band retention rate of 0.982 (Huyvaert and
Anderson, in press). Beginning in the 1992 –1993 breeding
season, steel bands were used instead, with an annual
retention rate of 1.00 (Huyvaert and Anderson, in press).
Between 1992 and 1995, all aluminum-banded birds also
received a steel band, so we consider band loss since 1993 to
be negligible. Resighting efficiency is 0.994 or greater
(Huyvaert and Anderson, in press). Young of the year were
not banded in the 1988 –1989 through 1991– 1992 breeding
seasons.
0531-5565/03/$ - see front matter q 2003 Elsevier Science Inc. All rights reserved.
doi:10.1016/S0531-5565(03)00104-9
758
D.J. Anderson, V. Apanius / Experimental Gerontology 38 (2003) 757–760
Almost all birds enter the breeding population by age 7
(Huyvaert, 1999). We conducted a longitudinal analysis of
survival of two known-age cohorts banded as nestlings in
the 1984 –1985 and 1985 – 1986 breeding seasons, respectively, by calculating the proportion of each cohort alive in
each band-resight survey relative to the number that was
alive at age 7 yrs.
life (13 – 16, $ 19) for evidence of senescent decline in
reproductive performance. In this article, we only consider
the analysis of the latter group but show the data for
comparison of reproductive success across the lifespan.
2.2. Actuarial senescence: cross-sectional analysis
3.1. Actuarial senescence
To conduct a cross-sectional analysis of annual survival,
we calculated the annual survival probability from the
beginning of the 2001 – 2002 breeding season to the
beginning of the 2002 – 2003 season. We used the knownage adults and two other groups banded as adults in 1984–
1985 and 1985– 1986 (assumed to be $ 4 yrs old at banding
(Huyvaert, 1999)) and so aged a minimum of 20 and 21 yrs,
respectively, in 2001 –2002. For these two groups (the
‘oldest adults’) we pooled sightings to increase the sample
size and the calculated transition probability is for birds
$ 20 yrs of age.
Survival probability showed little variation with age in
both longitudinal and cross-sectional analyses (Fig. 1). The
Weibel shape parameter was 0.137 ða ¼ 1:22 £ 1021 ^
2:80 £ 1021 ; b ¼ 25:99 £ 1022 ^ 9:29 £ 1021 Þ for the
1984– 1985 cohort, 0.076 ða ¼ 4:90 £ 1024 ^ 1:26 £ 1023 ;
b ¼ 1:97 ^ 9:78 £ 1021 Þ for the 1985 –1986 cohort, and
0.065 ða ¼ 2:71 £ 1023 ^ 8:99 £ 1023 ; b ¼ 1:17 ^ 1:22Þ
in the cross-sectional analysis. The median of these three
values (0.076) is plotted against the median m0 for the
three groups in Fig. 2, with the nine species that showed
model convergence in Ricklefs (1998). Over 20% of the
birds alive at age 7 were still alive at age 18.
3. Results
2.3. Actuarial senescence: parameter estimation
3.2. Reproductive senescence
Following Ricklefs (1998), we calculated the Weibull
parameter ðv ¼ a=ðb 2 1Þ; units of 1/time) based on the
equation mx ¼ m0 þ axb that relates age ðxÞ to age-specific
mortality ðmx Þ and the minimum mortality ðm0 Þ rate. The
latter can be interpreted as the mortality rate of young adults
before senescence, which largely reflects mortality from
extrinsic factors (Ricklefs, 1998). It was not possible to
estimate m0 directly from the data because the non-linear
estimation procedure did not converge or calculated a
negative value. Therefore, we used the minimum mortality
rate observed in each analysis, 0.0218, 0.0316, and 0.0667
for the 1984 –1985, 1985– 1986 and cross-sectional groups,
respectively.
The non-linear estimation procedure (PROC NLIN) of
SAS (SAS Institute Inc, Cary, NC; v. 8.2) was used for
fitting a and b parameters.
Reproductive performance improved with age for both
sexes at the beginning of the reproductive lifespan (Fig. 1).
After age 12, the probability of breeding was higher for
females (x2 ¼ 10:61 df ¼ 1; P ¼ 0:0011) than for males.
After controlling for differences between sexes, breeding
probability decreased with age ( x2 ¼ 10:69 df ¼ 4;
2.4. Reproductive senescence
Breeding of these same groups of birds was monitored
daily during the entire 2000– 2001 breeding season, and
each bird was scored for attempted reproduction (reached
the egg stage, yes/no) and successful fledging (produced an
offspring in juvenile plumage; yes/no). Breeding performance of birds known to be alive in that year was related to
age using logistic regression (PROC LOGISTIC of SAS) to
compare the fit of sequential models containing the intercept
only, sex, age, and the sex £ age interaction. We conservatively considered age as a categorical factor, especially
because the oldest adult group was not known-age. We
divided the analysis into early life (4 – 8 yrs) when
reproductive success was expected to improve and late
Fig. 1. Age-specific survival and reproduction of Nazca boobies.
Longitudinal survival histories of two cohorts (solid grey lines) and
cross-sectional transition probabilities between age classes (dotted grey
line) are associated with the left Y-axis. Reproductive performance of males
(dotted lines, 95% confidence intervals) and females (solid lines, 95%
confidence intervals) in the 2000–2001 breeding season is shown as the
proportion of living birds that attempted to reproduce (open circles) and the
proportion of breeding birds that fledged an offspring (closed circles).
Reproductive data are associated with the right axis. Reproductive data for
9 – 12 yr-olds are missing because young were not banded in the
corresponding years in the past. Males showed lower per capita
reproductive success than females did at most ages because the adult sex
ratio is strongly male-biased (unpub. data).
D.J. Anderson, V. Apanius / Experimental Gerontology 38 (2003) 757–760
759
age-related decline, but hatching success and especially
rearing of hatched offspring fell with increasing age (unpub.
data). For males, clutch size, hatching success, and rearing
success all showed age-related declines (unpub. data). Thus,
several components of reproductive performance may be
declining with age in Nazca boobies.
4.3. Reproductive senescence in long-lived seabirds
Fig. 2. Estimates of coefficients of Weibull functions fitted to the
relationship between mortality rate and age for Nazca boobies and for the
nine species in Ricklefs (1998) with fitted model convergence.
P ¼ 0:030). The interaction between sex and age was not
significant (x2 ¼ 5:06; df ¼ 4; P ¼ 0:28).
After the initial increase in probability of fledging (one
offspring by birds that attempted to breed) early in life,
females that bred were marginally more successful in
fledging offspring than males ( x2 ¼ 3:28, df ¼ 1;
P ¼ 0:07). After controlling for the difference between
sexes, fledging probability decreased with age (x2 ¼ 11:11;
df ¼ 4; P ¼ 0:025). Again, the interaction between sex and
age was not significant (x2 ¼ 3:42; df ¼ 4; P ¼ 0:49).
4. Discussion
4.1. Divergent rates of senescence
Nazca boobies appear to show the low rate of actuarial
senescence expected for pelagic seabirds, at least over the
age range available to us in this study and the heterogeneity
in the data which hampered estimation of the Weibel
parameter. Extrapolation of the survival curve suggests that
approximately 5% of birds alive as 7 yr olds will still be
alive at age 30 (Fig. 1). Evidence of declining reproductive
performance before age 20 was thus a surprising finding.
Our results are preliminary in the sense that reproductive
performance has been documented for only approximately
2/3 of potential lifespan, yet provides compelling evidence
that reproductive performance increases early in life and
then wanes in this long-lived seabird species.
4.2. Causes of reproductive senescence
The reasons for curtailed fledging success with age
among breeders in 2000– 2001 will be a focus of future
research, but some markers of reproductive senescence can
be analyzed with data in hand. The reproductive organs of
females showed little evidence of declining function with
age (Fig. 1), since they continued to lay eggs to age 19 þ .
Preliminary analysis of clutch size for females showed no
Studies of other long-lived seabirds show diverse
patterns of reproductive performance at advanced age. In
the short-tailed shearwater (Puffinus tenuirostris), the
probability of reproduction (incubating an egg) declined
monotonically with age for males but not females (reanalysis of Table 1 in Wooller et al., 1990), while fledgling
production from those eggs showed a step function decrease
with older age in males but not females (Wooller et al.,
1990). Fledgling production from eggs decreased in the
oldest cohort of wandering albatrosses (Diomedea exulans;
Weimerskirch, 1992), but not in kittiwake gulls (Rissa
tridactyla; Thomas and Coulson, 1988). However, hatching
rate appeared to decline in the oldest kittiwakes (Thomas
and Coulson, 1988). In the fulmar (Fulmarus glacialis),
reproductive performance was assessed in old birds prior to
their disappearance (i.e. presumed dead) compared to those
that continued returning to the colony and breeding. Birds
that did not return had decreased probability of laying eggs
and fledging offspring prior to their disappearance (Ollason
and Dunnet, 1988), suggesting that reproductive senescence
portends mortality. In contrast to these studies, egg and
fledgling production by very old common terns (Sterna
hirundo) did not decline with age, even in the oldest cohort
(Nisbet et al., 2002).
The simplest interpretation of these diverse outcomes is
that the selective factors acting on reproductive function are
independent from those acting on longevity (Ricklefs et al.,
2003). This contrasts with the prevailing paradigm (Partridge, 1987) that reproductive effort accelerates senescence
and mortality in a concerted fashion as suggested in the
fulmar study (Ollason and Dunnet, 1988). The alternative
perspective, supported by other avian taxa (Ricklefs, et al.,
2003), is that reproductive senescence and longevity are
effectively decoupled. A possible exception is that the
sustained physical performance required of foraging parents
may be a causal link between reproductive success and
longevity, as suggested in the fulmar study (Ollason and
Dunnet, 1988).
Unlike previous studies, we have little reason to believe
that anthropogenic factors (e.g. environmental contaminants, exploitation of marine resources, direct mortality
from long-line fishing (Sagar et al., 2000)), have influenced
the demography of our population. Therefore, some of the
problems that limit inferences about age-dependent reproduction and survival (Nisbet, 2001) are minimized in our
system, underscoring the importance of field studies of longlived seabirds in protected environments in order to
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D.J. Anderson, V. Apanius / Experimental Gerontology 38 (2003) 757–760
understand the evolutionary ecology of organisms with slow
aging.
5. Conclusions
Nazca boobies show the expected shallow decline in
survival with age, indicating a potential lifespan over
30 yrs. The probability of successful reproduction declines
with age more rapidly, suggesting the existence of a postreproductive lifespan in this species. Further study of the
oldest age classes will evaluate this possibility more
definitively. Nazca boobies offer an exceptional opportunity
for studying the nexus of physiological performance,
lifetime reproductive success, and aging because the
reproductive histories and age-structures are known from
our long-term studies.
Acknowledgements
Supported by National Geographic and NSF grants
(DEB 9304579, DEB 9629539, DEB 9726444) to D.J.A.
We thank the Galápagos National Park Service for
permission to work in the Park, the Charles Darwin
Research Station, TAME airlines, Galápagos Network,
and Ecoventura for logistical support, our many students,
technicians, and spouses for their contributions to the
fieldwork, and R.E. Ricklefs and A.A. Schuerlein for
comments on a previous draft.
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