AMER. ZOOL., 35:329-339 (1995)
Effects of Aging and Mate Retention on Reproductive
Success of Captive Female Peregrine Falcons1
N. J. CLUM
The Peregrine Fund, Inc., 5666 W. Flying Hawk Lane, Boise, Idaho 83709
SYNOPSIS. Separating ecological (extrinsic) factors affecting reproduction
from physiological and experiential (intrinsic) factors can be problematic
in free-ranging animals. This study examined age-related changes in six
measures of reproductive success (clutch size, fertility, hatchability, brood
size at hatching, survivorship of nestlings, and brood size at fledging) for
captive female peregrine falcons (Falco peregrinus) where ecological factors (i.e., access to mates, nesting sites, and food) were not limiting and
were similar across years and between individuals. Mean nestling survivorship increased throughout the lifespan of the female while all other
measures of reproduction peaked at about seven years of age and decreased
thereafter. Birds with prior breeding experience had higher productivity
than inexperienced birds of the same age. Productivity increased with
increasing experience of the pair. Productivity dropped by an average of
53% when females experienced a change of mate, and then subsequently
increased over a period of several years. Productivity was not affected
when birds were moved to different breeding sites. There was no evidence
that early improvements in reproduction were related to chronological
aging in the absence of experiential differences. Birds that began breeding
earlier produced more fledglings during their lifetimes as a result of higher
annual productivity. Lifetime reproduction was not correlated with longevity because birds with higher maximal egg production had shorter
breeding lifespans. Birds retaining mates produced more fledglings during
their lifetime than birds that changed mates, but birds that changed mates
more than once did not have lower lifetime reproduction than birds that
had only one mate change. These results suggest that 1) age-related changes
in reproduction are not necessarily resource-mediated, 2) in the absence
of resource limitation, experience of the pair is a primary factor determining annual reproductive success, 3) benefits of increasing experience
may be offset by the onset of senescence, 4) the cost of present egg production on future reproductive potential supports a "pleiotropic" theory
of aging, and 5) costs associated with mate changes may encourage selection for low "divorce" rates (i.e., lifetime monogamy) in this species.
bach, 1989; Mills, 1989). In birds with modg lifespans, however, there are
also clear
age-related changes in reproduction which generally follow a quadratic
function, increasing early in life and
decreasing later in life (Scott, 1988; Thomas
and
Coulson, 1988; Newton, 1988, 1989;
Owen and Black, 1989). Age-related changes
in reproduction may be influenced by chronological age, experience of an individual
• From the Symposium Reproductive Aging in Avian o r i t s m a t e > experience of the breeding pair
Species presented at the 21st International Ornithology together, or by temporal changes in COStS
and benefits of breeding. These factors may
Congress, Vienna, Austria in August, 1994.
329
INTRODUCTION
Much of the individual variation in annual
reproductive success of birds can be attributed to environmental factors such as the
availability/accessability of mates, territories, or food (Newton, 1979; Newton et al,
1983; Clum, unpublished data; Scott, 1988;
Bacon and Andersen-Harild, 1989; Gehl-
e r a t e t 0 lon
330
N. J. CLUM
influence reproduction directly, or indirectly by affecting access to resources. Distinguishing among physiological, ecological, experiential, and strategic factors is
difficult for wild birds because environmental variables cannot be controlled and birds
presumably reproduce at an optimal rate.
Age-related changes in six measures of
reproductive success (clutch size, fertility,
hatchability, brood size at hatching, survivorship of nestlings, and brood size at fledging) were examined for captive female peregrine falcons {Falco peregrinus). All females
were kept under similar conditions and were
not limited by access to mates, nesting sites,
or food, and it was therefore possible to
examine direct (non-resource-mediated)
effects of experience on reproductive performance. All females were also manipulated to produce eggs at their maximum rate,
allowing investigation of age-related changes
in physiological capacity of reproduction,
and tradeoffs between present and future
reproduction.
METHODS
Captive population
Reproductive data were analyzed from 21
captive, naturally copulating, female peregrine falcons that were paired in their first
year and retained throughout their reproductive lifetimes. Birds were paired on the
basis of genetic and management considerations; birds did not choose their own
mates. Pairs were housed together yearround in semi-enclosed outdoor chambers
exposed to ambient temperature and photoperiod in Fort Collins, Colorado, and Ithaca, New York. Birds held at the Colorado
facility were all F. p. anatum. Birds held in
New York included females of F. p. tundrius
(4), F. p. pealei (2), and F. p. brookei (2).
Following the 1984 breeding season, birds
from Colorado were transferred to Boise,
Idaho; following the 1985 breeding season
birds from New York were also transferred
to Idaho. Pairs at all sites were allowed to
incubate their eggs for approximately one
week to maximize hatchability (Burnham,
1983). Eggs were incubated artificially for
the remainder of the incubation period. Eggs
were weighed every two to three days,
adjusting incubator humidity to achieve a
total weight loss of 13-16% for the entire
incubation period, also to maximize hatchability (Heck and Konkel, 1991). Chicks
were hand-raised in the laboratory on
ground whole quail for 7-14 days. Chicks
were raised by adults (not necessarily their
parents) in semi-enclosed outdoor chambers for the remainder of the nestling period.
In the wild, peregrines normally produce
a single clutch of eggs (Cade, 1982). Reproduction of captive birds was maximized by
removing eggs. In 170 out of 193 bird-years,
egg production was maximized by removing completed clutches of eggs and allowing
the birds to re-lay (re-cycling). In 23 birdyears egg production was maximized by
removing individual eggs as they were laid
(extending).
Twelve of 21 females experienced at least
one change of mate during their lifetime;
four of these 12 birds experienced two mate
changes. Of sixteen total changes, five were
made as a result of the male dying, and the
remainder resulted from management decisions.
A breeding attempt was defined as any
year in which the female laid eggs. Fertility
was defined as ((fertile eggs/eggs laid) x 100).
Hatchability was defined as ((eggs hatched/
fertile eggs) x 100). Nestling survivorship
was defined as ((fledglings/hatched eggs) x
100). Productivity was defined as (number
offledglings/year).A failed breeding attempt
was defined as one from which no young
were fledged.
Statistical analysis
Patterns of reproductive success (clutch
size, fertility, hatchability, brood size at
hatching, survivorship of nestlings, and
brood size atfledging)across female age were
examined using a repeated measures analysis, including mate retention (whether or
not a female changed mates during her lifetime) and original breeding site (Colorado
or New York) as categorical variables. Single degree of freedom polynomial contrasts
from the repeated measures analysis were
examined to determine the shape of the
relation between dependent variables and
age. Female age and male age were highly
correlated for birds retaining mates (r2 =
0.979) and therefore an analysis of repro-
AGING AND REPRODUCTION IN FALCONS
100
I
CO
I
//
/
I
duction with respect to male age is not presented here.
Effects of breeding experience (experienced or not) and age on productivity, and
effects of experience with mate and number
of mates on productivity were analysed using
two-way ANOVAs. Short-term effects of
changing mates and changing sites on productivity (year pre-change vs. year postchange) were analyzed using paired Mests.
Independence of the maximal number of
eggs produced per year and age at first
breeding was determined using a G-test with
a Yates correction (Snedecor and Cochran,
1980). Relations between any two continuous variables were examined using regression analysis. Comparison of means between
two groups were made using the MannWhitney [/-statistic.
All proportional data (fertility, hatchability, nestling survivorship, mean productivity) were arcsine-transformed prior to
statistical analysis. Peregrines are normally
single-brooded (Cade, 1982) and therefore
reproductive data were analyzed only from
first clutches, with the exception of maximal
egg production. In cases where extended
birds produced more than four eggs, the
clutch was considered to consist of the first
four eggs laid. Only one captive female has
been observed to produce a clutch of more
than four eggs without manipulation (one
instance) in 25 years of captive breeding
experience with this species (C. Sandfort,
personal communication). Where the same
analysis was used on more than one dependent variable, results were corrected for
multiple comparisons using a sequential
Bonferroni method (Rice, 1989). Significance was assigned at the level of (corrected)
P < 0.05.
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RESULTS
/
Aging, experience, and reproduction
The average age at first breeding for
females was 3.4 yr (range 2-5, SD = 1.1)
and the mean age at last breeding was 12.7
yr (range 8-16, SD = 2.3). Over 90% of the
20
'.
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JL
2
3
4
5
Q
7
B
331
9
10 11 12 53 14 15 )6
FEMALE AGE (YR)
FIG. 1. A) Frequency of breeding relative to female
age. B) Proportion of failed breeding attempts relative
to female age. Q Causes of failed breeding attempts
relative to female age. Black bars indicate infertility,
cross-hatched bars indicate embryo death, hatched bars
indicate nestling death, and open bars indicates no
reproductive failures.
332
N. J. CLUM
TABLE 1. Summary of within- and between-group effects on aging and reproduction in female peregrines.*
Within
Clutch size
Fertility
Hatchability
Brood size
Survivorship
Number of
fledglings
Age
Age x mate
retention
< 0.00001
<0.00001
<0.00001
<0.00001
•cO.00001
<0.00001
Between
Age x site
Age x mate
retention x site
Mate retention
Site
Mate retention
x site
0.609
0.157
0.401
0.048
0.761
0.283
0.084
0.031
0.061
0.446
0.905
0.961
0.772
0.664
0.914
0.620
0.054
0.111
0.040
0.414
0.302
0.629
0.529
0.694
0.653
0.646
0.584
0.972
0.633
0.864
0.081
0.349
0.835
0.083
0.531
0.552
* Table of /"-values resulting from repeated measures analysis. The minimum P- value necessary for significance
with alpha = 0.05 and k = 6 are as follows: P, = O.O083, P2 = 0.01, P, = 0.0125, P4 = 0.017, />5 = 0.025, and
P6 = 0.05; where P, is the most significant of ranked F-values.
initial 21 females were still breeding at nine
years of age and over 25% were still breeding
at 15 years of age (Fig. 1A). Three females
(14%) lived beyond their ability to reproduce; one was euthanized at 19yr and two
at 18yr. The proportion of birds that
attempted to breed, but failed, was high
(> 40%) during the first two years and lowest
at ages 7-9. After 9 years, the proportion of
failed breeding attempts rose (Fig. IB).
Infertility was the primary cause of reproductive failure both early and late in the
reproductive lifetime, accounting for over
65% of failures at ages 2, 3, 11, and 13-16
(Fig. 1C). Failures resulting from embryo
death were the most consistent across ages
(mean, 20%). Failures resulting from nestling loss were only observed at ages 9 and
under.
There was a significant effect of female
age on all measures of reproductive success
(Table 1). There was no significant effect of
mate retention and/or site on the relation
between female age and any dependent variable. In all cases, the data were best fit by
a quadratic model (y = a + bx + ex2),
reflecting an initial increase in performance
and then a decrease with increasing age.
Mean annual fertility, hatchability, brood
size at hatching, and brood size at fledging
were generally higher at any given age for
females that retained their mates throughout their lifetimes than for females changing
mates (Fig. 2), but differences were not significant (Table 1). Mean annual reproduction did not differ between sites and there
were no significant interactions between site
and mate retention. Reproduction peaked
at seven years of age for all variables except
nestling survivorship, which increased
throughout the reproductive lifetime (Fig.
2).
Experienced birds had higher productivity than inexperienced birds (i.e., first time
breeders) at the same age, but productivity
did not change with age within these two
categories (Table 2). Mean productivity
dropped by 53% between the year preceding
a mate change and the first year with the
new mate (t = -2.419, P = 0.032), but
increased thereafter with the number of years
of experience with a mate for birds having
up to two mates; productivity decreased with
the number of mates for birds having one
or more years of experience (Table 3). The
degree of change in productivity was not
correlated with female age (rs = —0.380,
P > 0.20), female experience (rs = -0.503,
P = 0.10), age of new mate (r, = -0.246,
P > 0.20), or experience of new mate (rs =
-0.297, P > 0.20). Five of the 12 females
(42%) ceased breeding within one year after
changing mates; all five were 9 yr or older.
The remaining seven (58%) continued to
breed for at least three more years; these
females ranged in age from 4-9 yr. The mean
age of females with two or more mates was
greater than peak reproductive age (Table
4). Productivity did not change between the
year preceding a change of site and the first
year at the new site (t = -1.781, P = 0.095)
or increase with experience at a site (Table
5).
Maximal and lifetime reproduction
The maximum number of eggs obtained
from birds in their first year of breeding did
not differ between birds that were re-cycled
333
AGING AND REPRODUCTION IN FALCONS
100
10
15
20
10
15
20
120
120
5
FEMALE AGE (YR)
5
10
15
20
FEMALE AGE (YR)
FIG. 2. Age-related changes in reproduction of female peregrine falcons. Solid lines and circles represent females
retaining mates throughout their lifetime. Dashed lines and open circles represent females experiencing at least
one mate change during their lifetime. See Table 1 for significance levels.
334
N. J. CLUM
TABLE 2. Productivity of experienced and inexperienced female peregrines*
Age
o
Experienced
Not experienced
2.6 ± 1.7(5)
2.3 ± 1.4(12)
2.2 ± 1.6(16)
I.I ± 1.5(7)
1.0 ± 0.8(4)
1.4 ± 1.3(5)
* Mean number of fledglings ± one standard deviation. Sample sizes are in parentheses. Two-way ANOVA; Pv = 0.944, />„„ = 0.017, Pwzx, = 0.820.
and birds that were extended (U = 44.0, P
= 0.736). Maximal egg production followed
the same quadratic function as other agerelated variables (Fig. 3) but there was no
effect of age on maximal egg production in
the first year of breeding (Table 6). There
was a significant negative correlation
between the (maximal) number of eggs that
a female produced during her first three years
of breeding and the number of years that
she subsequently bred (Fig. 4). There was
no relation between egg production during
the first three years and subsequent mean
annual productivity (P = 0.966).
Although egg production from first
clutches was positively correlated with
length of breeding lifespan (Fig. 5A), lifetime reproduction (number of fledglings)
from first clutches was not correlated with
the number of breeding attempts (Fig. 5B)
or longevity (P = 0.875). Both lifetime
reproduction (Fig. 6A) and the frequency of
four-chick broods (Fig. 6B) were negatively
correlated with the age at first breeding.
There was no difference between females
that retained mates and females that changed
mates in age at first breeding (U = 53.0, P
= 0.941), number of breeding attempts (U
= 65.0, P = 0.430), or maximal egg production during the first three years of breeding (U = 45, P = 0.521). However, females
that retained their mates throughout their
lifetimes fledged marginally more young
5
10
15
20
FEMALE AGE (YR)
FIG. 3. Relation between maximal egg production and
female age.
from first clutches than females that experienced a mate change (meannochange = 23.2
± 8.7, meanchange = 17.4 ± 4.8, P = 0.059).
Lifetime reproduction of females that experienced two mate changes was not different
from females that experienced only one mate
change (mean, = 17.8 ± 5.0, mean2 = 16.8
± 5.0, P = 0.670). Maximal egg production
during the first three years did not differ
between females whose mates died, and
females whose mates were removed (U =
11.5, P = 0.919).
DISCUSSION
Intrinsic versus extrinsic factors
In many free-living avian species, only a
subset of the adult population may attempt
breeding in any given year (Clum, unpublished data; Newton, 1988, 1989; Ollason
and Dunnet, 1988). In contrast, captive peregrines generally bred every year (once they
TABLE 3. Effects of number of mates and experience with mate on productivity of female peregrines*
Years of experience with mate
Mate
0
1
2
3
1st
2nd
3rd
1.3 ± 1.4 (21)
0.8 ± 1.1 (12)
1.5 ± 1.3 (4)
2.2 ± 1.6(20)
1.6 ± 1.4(7)
0 .7 ± 1.2(4)
2.4 ± 1.3(17)
1.2 ± 1.6(6)
0.0
(1)
2.7 ± 1 • 3 ( 1 7 )
2.5 ± 1 .2(6)
* Mean number of fledglings ± one standard deviation. Sample sizes are in parentheses. Two-way ANOVA;
= 0.031, PC1P = 0.002, />„»_„ = 0.721.
m>a
335
AGING AND REPRODUCTION IN FALCONS
TABLE 4.
Age distribution of female peregrines relative tonumber of mates and experience with mates*
Years of experience with mate
:
Mate
0
1
2
3
1st
2nd
3rd
3.4 ± 1.4
7.9 ± 2.6
12.5 ± 1.9
4.4 ± 1.1
8.2 ± 2.6
13.5 ± 1.9
5.4 ± 1.0
8.1 ± 1.7
14.0
6.4 + 1.1
9.2 ± 1.8
Mean age of females in years ± one standard deviation. Sample sizes as in Table 3.
began) unless disturbed by a change of mate.
This high rate of breeding attempts in captive birds suggests that ecological factors are
probably the primary determinant of
whether or not a pair attempts to breed
(Newton, 1979). This suggestion is consistent with data showing egg production to be
related to protein/lipid reserves (Drobney,
1980) which are not limiting in the captive
population.
This study found all reproductive parameters except nestling survivorship to follow
a quadratic function with respect to female
age. This trend has been observed for clutch
size and brood size in several long-lived,
free-living avian species (Scott, 1988; Thomas and Coulson, 1988; Newton, 1988,
1989; Owen and Black, 1989). Observational and experimental studies have shown
reproductive output to be related to food
intake in a number of species (Nisbet, 1973;
Hogstedt, 1981;Dijkstra#a/., 1982; Clum,
unpublished data), and it has been suggested
that age-related changes in reproduction may
partly reflect changes in resource acquisition
over the lifetime of the individual (Newton,
1989). The similarity of reproductive patterns between wild and captive birds (not
limited by access to mates, territories, food,
and safe from predation) suggests that these
patterns may be of an intrinsic, rather than
an extrinsic (ecological), nature; i.e., they
may result directly from either physiological or experiential changes. This does not
imply that extrinsic factors are not impor-
tant in generating age-related patterns; it is
likely that physiological or experiential
changes may influence behaviors such as
foraging proficiency, and may accentuate
intrinsic patterns of reproduction.
Effects of physiological aging
Increases in reproduction early in life are
difficult to attribute to purely physiological
changes because birds presumably breed at
an optimal level. In an attempt to force
females to produce above their normal rate,
eggs were repeatedly removed. The failure
of this study to demonstrate a clear relation
between capacity for egg production and
increasing age of females would appear to
support the conclusion that there is no effect
of chronological aging on the capacity for
egg production. However, that conclusion
rests on the assumption that all birds of a
given age are physiologically equal, an
assumption that is probably no more true
for birds than for humans. Although it was
possible to modify reproductive output in
this study, it was not possible to manipulate
age atfirstbreeding. If individual birds began
to breed at a physiologically "appropriate"
age, differences in capacity for reproduction
among birds that first breed at different ages
would not be expected.
Decreases in reproduction late in life
(senescence) are generally assumed to be
physiological in nature, because older birds
possess adequate breeding experience.
Nestling survivorship is the one reproduc-
TABLE 5. Effects of site and experience at site on productivity of female peregrines.*
Years of experience at site
Site
2.3 ± 1.6(15)
2.3 ± 1.4(13)
2.5 ± 1.4(11)
1.5 ± 1.5(15)
Old
2.4 ± 1.4 (15)
1.5 ± 1.5(13)
2.7 ± 1.6(10)
2.3 ± 1.3 (10)
New
Mean number of fledglings ± one standard deviation. Sample sizes are in parentheses. Two-way ANOVA;
t = 0.737, />„,, = 0.095, />,;„.„„ = 0.176.
336
N. J. CLUM
10
20
30
40
EGG PRODUCTION (1ST 3 YRS)
40
B
FIG. 4. Relation between egg production during the
first three years of breeding and subsequent reproductive lifespan. r2 = 0.286, P = 0.012.
°
30 -_
a
o
tive variable measured here that is not directly
linked to the physiological condition of the
female. Both this study and studies of wild
European sparrowhawks (Accipiter nisus)
(Newton, 1989) have demonstrated that nestling survivorship is also the variable least likely
to decrease with age. Newton (1989) has suggested that survivorship may be the one variable that is effected primarily by experience;
concomitantly, the difference between the
pattern of survivorship and the pattern of
other reproductive variables may be our best
(indirect) evidence of senescence. The nestlings in this study, however, were not raised
by their own parents and therefore were not
directly influenced by their parent's experience. This suggests that either the correlation between survivorship and age of
female in this study is spurious, or that
experienced females produce hatchlings that
are intrinsically more likely to survive.
CD
s
"- 20 h
_
D
o
•
-~
o
a
LL
O
a:
m
m
3 10 h-
•
o
D
•
D
D
-
1
8
10
12
14
16
BREEDING LIFESPAN (YR)
FIG. 5. A) Relation between length of breeding lifespan and lifetime egg production from first clutches.
r2 = 0.674, P = 0.006. B) Relation between length of
breeding lifespan and lifetimefledglingproduction from
first clutches, r8 = 0.082, P = 0.207.
Effects and limitations of experience
Captive peregrines showed an increase in
productivity with experience of the pair
similar to that seen in short-tailed shearTABLE 6. Effect of age at first breeding on maximal waters (Puffinus tenuirostris) (Wooler et al,
egg production of female peregrines*
1989). Higher productivity in more experienced captive birds suggests that the
Number of eggs per year
Age at first breeding
advantage of experience lies at least par5.2 ± 3.2 (5)
tially in the nature of the pairbond itself and
4.6 ± 1.9(7)
need not be resource-mediated. Change of
7.0 ± 3.3 (4)
breeding site failed to produce the dramatic
7.6 ± 3.0 (5)
* Mean number of eggs per year ± one standard drop in productivity associated with a
deviation. Sample sizes are in parentheses. One-way change in mate, indicating a difference
ANOVA, P = 0.253.
between disturbance within the pairbond
337
AGING AND REPRODUCTION IN FALCONS
and a disturbance between the pair and the
environment. Peregrines in this study did
not choose their mates, and therefore
decreases in reproduction associated with a
new mate could be artificial or artificially
large. However, similar drops in reproduction of comparable magnitude also occur in
some (but not all) species of wild birds that
experience a change of mate (Scott, 1988;
Owen and Black, 1989; Wooler et al, 1989).
Stability of pairbonds appears to be reflected
in the physiology of individuals (Clum et
al, unpublished data), and this may provide
a mechanism by which productivity is
increased or decreased.
Unlike shearwaters, productivity of peregrines only increased with experience for
the first two mates, and actually decreased
with experience for the third mate. This
decrease was probably related to the
advanced age of female peregrines with a
third mate (mean, 12.5 yr), which was well
beyond the peak reproductive age (mean, 7
yr). The substantial increase in age of females
between subsequent mates also precluded
detection of an increase in productivity with
increasing individual experience similar to
that observed by Wooler et al. (1989) in
shearwaters. The large proportion (83%) of
older (9+ yr) females that ceased breeding
following a mate change suggests that such
disturbances may be particularly severe for
older females. The absence of a difference
in lifetime reproduction between birds
experiencing two mate changes and birds
experiencing three mate changes may indicate that senescence is more limiting than
pair experience at advanced ages.
As the proportion of failed breeding
attempts climbed with age (after seven
years), so did the proportion of failures
resulting from infertility. Infertility in young
pairs is generally suggested to reflect a lack
of synchrony between members of the pair.
While a breakdown of synchrony as pairs
age is not impossible, it may be more likely
that reduced fertility results from declining
quality of gametes, either eggs or sperm.
Although our analysis is presented in terms
of female age, the high correlation between
male and female age in this data set means
that a decrease in fertility (or any other variable) may also occur as a result of increased
age of males.
1
2
3
4
5
AGE AT FIRST BREEDING (YR)
FIG. 6. A) Relation between lifetime fledgling production and age at first breeding, r2 = 0.223, P = 0.031.
B) Relation between frequency of four-chick broods
and age at first breeding, r2 = 0.291, P = 0.012.
Lifetime reproduction
Age at first breeding of captive female
peregrines was about a year later than the
two to three years recorded for this species
in the wild (Cade, 1982; Mearns and Newton, 1984). This delay in breeding compared
to wild birds could be related to stresses
associated with captivity, methods of rearing, or inability of birds to choose mates,
resulting in greater incompatability within
pairs. Not surprisingly, peregrines in captivity also tended to live longer than wild
birds. Most wild peregrines that survive to
breed probably do not live past five years
338
N. J. CLUM
of age (Yates et al, 1988); this correlates
fairly well with the observed onset of senescence in captive birds, which occurs after
about seven years of age. However, the
maximum documented longevity of wild
peregrines is 17 yr (Newton, 1979). Given
that breeding lifespan of captive birds was
reduced in response to the level of maximal
egg production, onset of senescense in nonmanipulated birds may occur later than in
this population.
Newton (1989) found a negative relationship between age at first breeding and lifetime reproduction in sparrowhawks, with
birds that bred earlier producing more young
than those breeding later. Captive birds that
began breeding at younger ages had higher
lifetime reproduction, but not because these
birds had longer breeding lifespans; birds
that bred earlier were more likely to produce
the maximum number of fledglings (4 per
attempt) than birds that bred later. The
observed relation between early onset of
breeding and improved breeding in captive
birds may be the equivalent to moving to a
"new" (captive) environment, where certain individuals may enjoy a reproductive
advantage. Suitability to a new environment might well be reflected in both the
ability to breed early (in this case, at an age
more similar to wild birds) and to breed
better overall. If physiological "readiness"
were linked to reproductive ability in wild
birds, we would expect selection to favor
early breeders, and variation in age at first
breeding to be governed primarily by
resource availability.
The significant relation between egg production and longevity is not suprising since
females produced four-egg clutches in 78%
of all breeding attempts. In contrast to
almost every longterm study of long-lived
free-ranging avian species, however, this
study found no relation between lifetime
reproduction (fledgling production) and
longevity (see references in Clutton-Brock,
1988 and Newton, 1989). This discrepancy
is most likely related to the maximized egg
production of our population. Birds with
higher egg production early in life breed for
fewer years, and therefore ultimately produce a similar number of fledglings compared with birds that produce at a lower rate
for a longer period of time. These results
demonstrate a clear cost of present egg production to future reproductive potential, and
are consistent with a "pleiotropic" theory
of aging: mutations that encourage senescence are selected for because of a related
increase in reproduction earlier in life (Williams, 1957; Hamilton, 1966; Partridge,
1989). The absence of a correlation between
maximal egg production and subsequent
annual productivity suggests that higher
production does not change either the quadratic nature of the relation between productivity and age or limit the level of production in any given year, but results in an
earlier onset of senescence.
Effects of mate change
Although the average annual productivity
of birds that changed mates was not significantly lower than birds retaining mates, our
results suggest that the cumulative effect of
mate change is to depress lifetime reproduction. Unlike birds that differed in age of
first breeding, the difference in lifetime
reproduction does not appear to be attributable to a difference in the quality of birds
since there was no difference between groups
in onset, initial level, or longevity of reproduction; i.e., mates were not changed because
the pair performed poorly. The annual turnover rate of wild peregrines has been estimated in three populations at between 11
and 23% for each sex, and therefore the
probability of either member of the pair disappearing during a reproductive lifespan of
three years (assuming an age at first breeding
of two years) is 39-42%. The difference in
lifetime reproduction between birds changing mates and birds retaining mates could
actually be greater in wild populations
because the effect of the change is diluted
over a shorter breeding lifespan (3 yr vs. 9
yr) than in captive birds. Wild peregrines
are known to "divorce" occasionally
(Mearns and Newton, 1984; Ambrose and
Riddle, 1988; Enderson and Craig, 1988)
and therefore the rate of turnover in pairs
is greater than that expected from mortality
alone. However, if mate change in wild birds
is accompanied by decreases in reproductive success, as is seen in captive birds and
wild birds of other species, it is to be expected
AGING AND REPRODUCTION IN FALCONS
that selection would favor lifetime monogamy in this species.
ACKNOWLEDGMENTS
I would like to thank J. Beltoff and C.
Watson for discussions regarding statistical
analyses, and T. Cade, J. Linthicum, and I.
Newton for comments on the manuscript.
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