AMER. ZOOL., 35:318-328 (1995)
Stages of Age-Related Reproductive Success in Birds: Simultaneous
Effects of Age, Pair-Bond Duration and Reproductive Experience
GENE S. FOWLER
Department of Biology, Pomona College, 609 N. College Ave., Claremont California 91711
SYNOPSIS. Most organisms reproduce episodically rather than continuously. Forms of discontinuity may include seasonal breeding in annual
cycles, and delayed breeding and/or senescence over the lifespan of individuals. In addition, age can have profound effects on the annual reproductive success (RS) of a wide variety of animals. Explanations of the
effects of age on RS can be confounded, however, by the acquired breeding
experience of individuals, and the duration of pair-bonds, both of which
have effects on RS similar to those of age itself. However, most studies
of the effects of age on RS prior to senescence have not accounted for the
effects of pair-bond duration, and many have treated age and experience
as synonyms. In this paper I summarize the effects of all three factors,
discuss the simultaneous and interrelated nature of their effects, and suggest ways to separate the relative contributions of each.
mals, and may include larval forms, instars,
a period of growth to attain adult body
or
What proportion of its lifetime should an
size.
But, in many cases, organisms that have
organism devote to reproduction? This
question is one of the implicit bases under- reached adult body size further delay the
lying life history theory (Cole, 1954; May- onset of reproduction (e.g., Newton 1989,
nard Smith, 1978; Charlesworth, 1980). papers therein). Seasonal breeding, in which
From a simplistic Darwinian perspective, reproduction occupies only a part of each
the answer would be that an organism should annual cycle, is another widespread form of
reproduce continuously from birth until reproductive discontinuity that has been
death, and furthermore, at the maximum extensively studied (Lack, 1966; Perrins,
rate of which the organism is capable (Par- 1970; Murton and Westwood, 1977).
tridge, 1989). Such a strategy would maxi- Finally, some organisms (typically animals
mize the fitness of individuals relative to with relatively long lifespans) show reprothose individuals that follow any other ductive senescence, the cessation of breedstrategy, assuming equal lifespan and fecun- ing before the end of the lifespan (papers in
dity. However, few if any organisms employ this symposium).
Many of the species that show reproducsuch a reproductive strategy; individuals
spend parts of their lives engaged in activ- tive senescence also delay the onset of
ities other than reproduction. Reproduction breeding, and the first few breeding attempts
is inherently discontinuous and reproduc- are often less successful than subsequent
tive performance cannot be maximized at attempts. The result can be a general pattern
all stages of the life of the individual (Par- of lifetime reproductive performance for a
population or species similar to that depicted
tridge, 1989).
in
Figure 1, where there are 4 distinct phases:
The forms of discontinuity are varied. A
1)
delayed
breeding, when the annual fitness
delay between birth (hatching, or fertilizais zero and no reproduction is
increment
tion in some forms) and the onset of reproattempted;
2) onset of breeding, when the
duction is typical among plants and aniannual increment of fitness increases each
year until 3) adult breeding, the mean annual
reproductive success of experienced adults,
' From the Symposium Reproductive Aging in Avian and finally 4) reproductive senescence, when
Species presented at the 21 st International Ornithology
the annual increment of fitness decreases,
Congress, Vienna, Austria in August, 1994.
INTRODUCTION
318
319
AGE, PAIR-BONDS AND RS IN BIRDS
perhaps reaching zero before individuals die.
Not all species experience all four phases,
and the RS experienced by individuals of
any particular species may vary considerably from the population mean, but the general sequence is widespread among iteroparous animals. The first phase (delayed
breeding) has been the subject of much theoretical and empirical development (Cole,
1954; Gadgil and Bossert, 1970; Curio,
1988), and will not be considered here.
Senescence is the subject of the other papers
in this symposium, and here I focus on the
second and third phases, on the factors that
influence the ontogeny of reproductive performance after the onset of breeding, and
that influence the annual fitness increment
of experienced adults.
Studies of the effects of age on RS in young
and mature adults can be confounded with
two other variables, however: duration of
the pair-bond and acquired breeding experience. Chronological age and breeding
experience are tightly linked but not identical. Also, many avian species that show a
clear relationship between age and RS also
form long-term pair-bonds (LTPBs), which
are themselves positively correlated with RS
(Rowley, 1983; Mock and Fujioka, 1990).
In many species with LTPBs, experienced
adults in newly-formed pairs (due to divorce
or loss of mate) have decreased RS, as
depicted by the dotted line in Figure 1. My
goal in this paper is to describe the separate
and combined effects of age, experience and
pair bonds on RS, in particular their simultaneous co-occurrence, to discuss hypotheses that explain the effects of each, and to
identify gaps in the current state of knowledge.
AGE AND THE DEVELOPMENT OF
REPRODUCTIVE PERFORMANCE
Reproductive success, and a number of
its components, are strongly associated with
increasing age in a variety birds (Lack, 1966;
Ryder, 1980; Saether 1990; Table 1). Documented factors that underlie the increased
RS of older birds include earlier laying in
seasonal breeders, larger clutch and/or egg
size and better coordination of parental
duties.
V)
r
I
•L
- -
m
\
- AGE w RS
AGEvsRSw' MATE CHANGE
IV
\
CHRONOLOGICAL AGE
FIG. 1. Stages of age-related reproductive success (RS)
in birds. I.) Delayed Breeding. II.) Improving performance after onset of breeding. III.) Experienced adulthood. IV.) Senescence. Not all species exhibit all four
stages. Dotted line indicates the RS of pairs that have
changed mates in many species that maintain longterm pair bonds.
Age and laying date
Older females tend to lay eggs earlier in
the breeding season in a wide variety of species, including procellariiforms (Ollasen and
Dunnett, 1978; Rechten, 1986), waterfowl
(Baillie and Milne, 1982; Hamann and
Cooke, 1987), charadriiforms (Coulson and
White, 1958; Coulson and Horobin, 1976),
pelecaniforms (Blus and Keahy, 1978; Potts
etai, 1980) gruiforms (Crawford, 1980) and
passerines (Dhondt, 1989; Wheelwright and
Schultz, 1994; Table 1). Female age is the
primary determinant of laying date, but
increasing male age is independently associated with earlier laying dates in some species (e.g., Thomas, 1983). Differences in laying date between older and younger birds
range from a few days (Hamann and Cooke,
1978; Dhondt, 1989) to as much as 5 weeks
(Potts et al, 1980). Early laying is positively
correlated with both survival of chicks to
fledging and recruitment into the breeding
population (Perrins, 1970).
Age and eggs
Both clutch size and egg size are positively
correlated with age in many species. Clutch
size is larger in older birds in most species
that show age effects on laying date [e.g.,
Finney and Cooke, 1978; Haymes and
Blokpoel, 1980; Pugesek and Diem, 1983;
Table 1). Increased clutch size is strongly
correlated with higher fledging success [e.g.,
Perrins and McCleery, 1985) Egg size has
been less commonly studied, but also shows
320
GENE S. FOWLER
TABLE 1. Components of reproductive success (RS) that lead to higher overall RS in birds and that have been
attributed to the effects of increasing age (AGE), experience as a breeder (EXPERIENCE), or pair-bond duration
(PAIR-BOND).*
RS component
AGE
Courtship behavior
Laying date (hatch
date in some cases)
14*, 18, 22, 26, 27, 29,
30, 32, 33, 34, 35, 36,
37, 38, 40, 42, 43, 47,
55, 57, 60, 61, 64
Clutch size
14,18,22,24,26,27,28,
29, 30, 33, 34, 36, 37,
39, 43, 44, 48, 49, 52,
53, 54, 57, 64, 74
Egg size
17,28,30,31,32,48,49,
50, 54, 74
Coordination of paren- 21
tal duties
Nest site quality
4, 27, 37, 42, 44, 45
Overall RS
1,6,14,18,22,23,25,
27, 28, 29, 30, 35, 38,
40, 43, 44, 45, 46, 49,
53, 54, 56, 57, 58, 59,
60, 61, 62, 65, 66, 74
No effect on RS
70,71
EXPERIENCE
4, 6, 16, 17, 19, 23, 56
1,4,58,60,61,77
PAIR-BOND
3, 8
4, 5, 6, 9, 17, 18, 19, 21,
22, 23, 49
1,4,5,13,14,18,22,24,
75
12,31,56
51
24
15,17,21
23
1,2,4,6,7,8,17,19,42,
46, 56, 58, 61, 63
70
1,2,4,5,6,7,8,9,10,
11, 14, 17, 18, 19, 20,
21, 23, 49, 62, 66, 75,
76
67,68,69,72,73
* Numbers refer to "Sources listed below. All components are positively correlated with AGE, EXPERIENCE
and PAIR-BOND, except courtship behavior and laying date, which are negatively correlated. Note that age
and experience have often been treated synonymously in the literature; references in this Table are placed in
the category to which the author(s) attributed the RS component.
** Sources-1) Bradley et al. (1990) 2) Bradley et al. (1995) 3) Chardine (1987) 4) Coulson (1970) 5) Coulson
(1978) 6) Ens et al. (1993) 7) Fisher (1976) 8) Nelson (1970) 9) Kepler (1969) 10) Newton and Marquiss (1982)
11) Ollasen and Dunnett (1985) 12) Ollasen and Dunnett (1983) 13) Parmalee and Pietz (1987) 14) Perrins and
McCleery (1985) 15) Sedinger and Raveling (1990) 16) Pietiainen (1988) 17) Brooke (1978) 18) Coulson (1966)
19) Davis (1976) 20) Emslie et al. (1992) 21) Fowler (1993) 22) Mills (1973) 23) Ollasen and Dunnet (1978)
24) Cooke et al. (1981) 25) Ainley and Schlatter (1972) 26) Baillie and Milne (1982) 27) Blus and Keahy (1978)
28) Coulson and Horobin (1976) 29) Coulson and White (1958) 30) Crawford (1980) 31) Croxall et al. (1992)
32) Davis (1975) 33) Dhondt (1989) 34) Finney and Cooke (1978) 35) Fisher (1975) 36) Hamann and Cooke
(1987) 37) Haymes and Blokpoel (1980) 38) Kluijver (1951) 39) LeResch and Sladen (1970) 40) Nol and Smith
(1987) 41) Pietiainen (1988) 42) Potts et al. (1980) 43) Pugesek (1983) 44) Pugesek and Diem (1983) 45) Ralph
and Pearson (1971) 46) Raveling (1981) 47) Rechten (1986) 48) Richdale (1949) 49) Nice (1937) 50) Richdale
(1955) 51) Richdale and Warham (1973) 52) Rockwell et al. (1983) 53) Reskaft et al. (1983) 54) Thomas (1983)
55) Van Ryzin and Fisher (1976) 56) Weimerskirch (1990) 57) Wheelwright and Schultz (1994) 58) Wooller et
al. (1990) 59) Smith (1988) 60) Bryant (1988) 61) Harvey et al. (1988) 62) Scott (1988) 63) Fitzpatrick and
Woolfenden (1988) 64) Postupalsky (1989) 65) Gehlbach (1989) 66) Owen and Black (1989) 67) Baeyens (1981)
68) Beletskey and Orians (1989) 69) Freed (1987) 70) Furness (1984) 71) Hannon and Smith (1984) 72) Harris
et al. (1987) 73) Marzluffand Balda (1988) 74) Shaw (1986) 75) Spurr (1975) 76) Wood (1971) 77) Dann and
Cullen (1990).
a positive correlation with age in some species (Richdale, 1955; Davis, 1975; Crawford, 1980). However, the importance of egg
size as an influence on fledging success has
been less often studied than clutch size, and
is not entirely clear, even within a single
species. Parsons (1970) found that in the
Herring gull {Larus argentatus) egg size was
positively correlated with chick survival,
whereas Davis (1975), studying the same
population, attributed the correlation to the
effects of age and experience of the parents.
In general, clutch size appears to be a much
more important determinant of RS.
*& and Parental duties
Parental duties include incubation,
brooding, and chick feeding or guarding. Few
studies have directly examined the relationship between age and parental duties, but
Ainley and Schlatter (1972) attribute chick
raising ability to increasing age, and Coul-
AGE, PAIR-BONDS AND RS IN BIRDS
321
son (1966) and Coulson and White (1958) (i.e., laying dates, clutch size and overall RS;
suggested that older birds had better coor- Table 1).
dination of incubation turns. Improved
coordination should act to improve hatch- Hypotheses to explain age effects
ing success and chick growth, as well as to
Curio (1983) described two hypotheses
minimize reproductive costs for one or both (not mutually exclusive) to explain the
observed age-related increases in RS. Here,
parents.
I recast those hypotheses in the light of more
recent work on reproductive effort and
Age and foraging success
residual reproductive value (see also Nol
Age is positively correlated with foraging and Smith, 1987; Sasther, 1990).
success in many bird species (see Wunderle
Constraint hypothesis —Under this
[ 1991 ] for review). Most studies have exam- hypothesis young birds reproduce less well
ined differences between adults and non- because they are limited by incomplete
breeding juveniles (e.g., Orians, 1969; acquisition of necessary skills (such as forRecher and Recher, 1969), but age can also aging), or incomplete physiological matuinfluence foraging success in breeding adults ration. A subsidiary of this hypothesis is
(Ainley and Schlatter, 1972). Although that some birds may be inferior, with both
causal links have not been identified, for- lower RS and lower survivorship. Their
aging success probably has a strong influ- deaths would necessarily inflate the mean
ence on laying date and clutch or egg size. RS of surviving birds in subsequent years.
Better foragers are also likely to be more Curio (1983) treated this possibility as a
able to feed offspring, and therefore to have separate hypothesis from the maturation
higher reproductive success, as well as higher hypothesis, but both are forms of consurvival and longer lifespans.
straint. There have been few tests between
these two possibilities, but Hamann and
Reproductive experience
Cooke (1987) found the maturation hypothIn addition to pure age effects, the accu- esis to be better supported.
mulated experience of a breeding adult can
Restraint hypothesis. —Under this
influence its reproductive success. Age and hypothesis, young birds expend less effort
experience are obviously strongly corre- in reproduction than older birds, and therelated, as experience cannot be acquired fore have lower RS. Here, young birds do
without also increasing age, but the two are not lack skills and are as capable as older
not identical. An animal could be of birds, but produce fewer young as a result
advanced age, yet have no breeding expe- of balancing the costs of current reproducrience because it has never attempted to tion against the probability of future RS. If
breed. The two terms (age and experience) reproduction is costly in terms of survival
have sometimes been used interchangeably and future RS, then animals should modin the literature, but their effects are poten- ulate their current reproductive effort so as
tially separable. The effects of experience to maximize their lifetime RS (Charlescan be elucidated by comparing the RS of worth, 1980). Saether (1990) reviewed the
animals of identical age but varying expe- effects of age on RS and concluded that
rience, whereas the effects of age can be although there is evidence in support of both
identified by comparing animals of different constraint and restraint hypotheses, that
age at the time of first breeding. Few studies there was more evidence in support of the
have attempted such an analysis, but those constraint hypothesis. Young birds are genthat did have generally shown that both erally less capable rather than less willing.
chronological age and breeding experience
are positively correlated with RS (Bradley
PAIR-BOND DURATION AND
et al, 1990; Emslie et al, 1993). The comREPRODUCTIVE PERFORMANCE
ponents of RS that are affected by experiLong-term pair-bonds (LTPBs) are an
ence are similar to those affected by age alone
extreme form of monogamy, in which one
322
GENE S. FOWLER
male and one female reunite for two or more
successive breeding seasons (note that double-brooding—two clutches in one breeding
season—is not a long-term pair-bond in this
sense; LTPB refers to mate fidelity between
breeding seasons). Such high mate fidelity
is distributed widely within the Class Aves,
occurring in many orders but primarily in
long-lived species (Rowley, 1983). Although
LTPBs occur in some passerines (e.g., Perrins and McCleery, 1985; Dhondt, 1989),
they appear less common than in other
orders (Rowley, 1983), especially at temperate latitudes. This is perhaps because of
the short life spans of temperate zone passerines. Many tropical passerines have long
lifespans and are considered to maintain
LTPBs (Kunkel, 1974) but there have been
few definitive studies of mate retention in
tropical species.
LTPBs are commonly associated with
higher RS in pairs that reunite between years
compared to newly-formed pairs (Rowley,
1983; Mock and Fujioka, 1990), although
some species maintain LTPBs that are not
associated with increased RS (e.g., Freed,
1987; Marzluffand Balda, 1988). Components of RS that are also correlated with
mate retention include: less time spent in
pre-laying behaviors, earlier laying date
within the breeding season, larger clutch size,
and better coordination of parental duties
(Table 1).
LTPBs and prelaying behavior
In some species with LTPBs, continuing
pairs lay earlier in the season, but do not
necessarily arrive earlier at breeding sites
(Chardine, 1987). This suggests that faithful
pairs spend less time in prelaying activities
such as courtship, but there have been very
few studies of this prediction. Chardine
(1987) found that kittiwakes (Rissa tridactyla) in newly formed pairs spent more time
at the nest site and engaged in more greeting
behaviors than continuing faithful pairs, and
Nelson (1970) described lower rates of
aggressive behavior (but more intense
courtship behavior) between partners within
continuing pairs of gannets (Morus bassanus). However, these are the only two
studies that directly demonstrate such a
relationship.
LTPBs and laying date
In some species that maintain LTPB's,
continuing pairs lay earlier in the breeding
season than newly-formed pairs (Coulson,
1966; Kepler, 1969; Mills, 1973; Brooke,
1978; Table 1). Laying dates are not influenced by pair-bond duration in all species
however (Cooke et al, 1981; Newton and
Marquiss, 1982), even when RS is higher in
continuing pairs. In addition, the range of
differences appears smaller than that for agerelated effects, and is typically no more than
a week (Mills, 1973; Ollassen and Dunnett,
1978). Age appears to have a stronger influence on the initiation of clutches than does
pair-bond duration.
LTPBs and Eggs
Females in continuing pairs often lay
larger clutches in species with LTPB's
(Coulson, 1966; Spurr, 1975; Cooke et al.,
1981; Perrins and McCleery, 1985; Table
1). There is no independent effect of the
male; by definition both sexes are present
in a continuing pair. However, egg size has
been found to be correlated with pair bond
duration in only one study (Richdale and
Warham, 1973), but most LTPB studies
have not reported egg measurements.
LTPBs and parental duties
As was the case for age-effects on parental
behavior, the relationship between LTPBs
and parental behavior has been little studied. Brooke (1978) suggested that newly
formed pairs of Manx Shearwaters (Puffinus
puffinus) had poorer coordination of incubation turns. Cooke et al. (1981) found that
continuing pairs were more attentive to their
clutch at the time of hatching in Snow Geese
(Anser caerulescens), and Fowler (1993)
showed that members of faithful pairs shared
chick-brooding and feeding turns more
evenly than newly formed pairs of Magellanic Penguins (Spheniscus magellanicus),
but I have found no other studies in this
category. Studies of parental behavior would
likely be a fruitful means of identifying the
AGE, PAIR-BONDS AND RS IN BIRDS
mechanisms underlying LTPB-associated
increased RS.
Hypotheses to explain pair-bond effects
Here, I propose two hypotheses that can
explain the increased RS associated with
LTPBs. They are not mutually exclusive,
and there is evidence for both.
Assured-age hypothesis.—If a bird can
recognize the identity of individuals but not
assess the age of unfamiliar individuals, then
retention of a mate across years can be a
means of assuring high reproductive performance in the future, and long-term pair
bonds could be explained on the basis of
age effects. In this view, LTPBs are merely
a side-effect of the correlation between age
and RS, and have no influence per se on
RS. Pair bonds should be easily formed, and
formation should incur no costs in terms of
current or future RS. In some cases, birds
seem to be able to assess the age of strangers
{e.g., Potts et al., 1980), and there is strong
age-based assortative mating as well as a
very high (>75%) annual divorce rate. In
other species, there is little age-based assorative mating and age assessment appears to
be difficult (Reid, 1988).
Pair-bond investment hypothesis. —If the
formation of pair bonds requires an investment of time, energy or other ecological currency that is not required of established
pairs, that investment would be lost when
pairs split, and the need to reinvest would
explain the reduced reproductive success of
newly formed pairs. This hypothesis is an
extension of the idea that familiarity with a
mate is the source of the increased RS associated with LTPBs (Lehrman, 1965; Coulson, 1966). Acquisition of familiarity
requires an investment of time, but other
forms of investment may also be required
to form a pair bond (e.g., energy spent in
courtship or nest building, courtship feeding, etc.).
SPECIES WITH NO AGE OR PAIR-BOND
EFFECTS ON RS
Not all avian species with long lifespans
and/or long-term pair-bonds show a correlation between these factors and RS (Table
1). In some species, neither age nor pair-
323
bond duration affects RS {e.g., Blue-Eyed
Shags Phalacrocorax atriceps, Shaw, 1986),
but most studies have focused on one factor
or the other. Age and experience were not
correlated with RS in Great Skuas (Catharacta skua, Furness, 1984) and Willow Ptar-
migan (Lagopus lagopus, Hannon and
Smith, 1984). Pair-bond duration was
uncorrelated with RS in Pinyon Jays (Gymnorhinus cyanocephalus, Marzluffand Balda,
1988), House Wrens {Troglodytes aedon,
Freed, 1987), and Oystercatchers (Haematopus ostralegus, Harris et al., 1985). In some
cases, mate fidelity is related to territory
quality (Baeyens 1981) or familiarity with
the territory and its neighbors (Beletsky and
Orians, 1988). Here, the mates are being
faithful to the territory or surrounding conditions rather than to each other. Finally,
the preceding cases are only those where age
or pair-bond effects were looked for but not
found. One looks for effects where one
expects to find them, and there are likely
many more species where age and pair-bond
duration have little effect on reproductive
performance.
COMBINED EFFECTS OF AGE AND
PAIR-BONDS
The effects of age (with its covariate,
experience) and pair-bond duration are not
mutually exclusive; both can influence
reproductive success simultaneously (e.g.,
Coulson, 1966; Mills, 1973; Ollasen and
Dunnett, 1978; Perrins and McCleery, 1985;
Bradley et al., 1990; Weimerskirch, 1990;
Wooller et al., 1990). Seventeen of 29 pairbond related papers examined in detail for
this review found simultaneous effects of
both age and pair-bond; the other 12 did
not address the issue of age. The combined
effects are complex, with interactions not
only between age and pair-bond, but
between some of the components of RS as
well (Fig. 2).
However, the influence of age and pairbond on the components of RS can be separated and identified. If only age-effects were
to occur, then any pairing between experienced older birds should have equivalent
higher success, regardless of prior duration
of the bond. Similarly, if only pair-bond
324
GENE S. FOWLER
RS
A
CHICK
GROWTH
PARENTAL
BEHAVIOR
HATCHING
SUCCESS
FORAGING
SUCCESS
PRE-LAY
BEHAVIOR
AGE/
EXPERIENCE
CLUTCH/
EGG SIZE
PAIR-BOND
DURATION
FIG. 2. Interrelationships between age/experience, pair-bond duration and the components of reproductive
success. Arrows indicate directional relationships that have been documented (refs. in Table 1), but are not
necessarily causal links.
effects were to occur, then any newly-formed
pair should have equivalent lower success,
regardless of the age of the individuals
involved. If both effects occur, then pairs
that remain faithful across years, newlyformed pairs of older experienced birds, and
pairs with younger birds should decline in
RS, or in components that contribute to sue-
AGE, PAIR-BONDS AND RS IN BIRDS
cess, in that order. Ideally, one should study
four types of pairs: 1) continuing pairs of
experienced breeders, 2) pairs of experienced breeders that are newly-formed pairs
as a result of divorce or loss of mate, 3) pairs
where both members are young, first-time
breeders, and 4) pairs where one mate is
experienced and the other is a first-time
breeder. If the first-time breeders are of different ages, then the relative effects of age
and experience can also be identified as the
success of pairs is monitored through time.
FUTURE DIRECTIONS
The difficulty with studies of the effects
of age and pair-bond duration is that they
require detailed long-term field studies (e.g.,
Lack, 1966; Newton, 1989). Age/experience
effects have been considerably more often
studied than pair-bond effects (Table 1), but
most studies of age-effects do not account
for possible effects of pair-bond duration in
their analysis. The relative contribution of
each factor to overall RS has not often been
separated even in combined studies. More
information on the effects of pair bonds is
needed, and in particular, tests of explanatory hypotheses. There is currently little
information available on the effects of either
age or pair-bonds on sexual and parental
behavior (Table 1), and much more is
needed.
Lastly, the mechanisms underlying age
and pair-bond effects on RS are poorly
understood. Do older birds remain in better
physiological condition than younger birds?
Are they simply exploiting greater knowledge about the surrounding environment,
or are changes in RS solely due to changes
in reproductive effort as the residual reproductive value of individual changes over
their lifespan? What is the physiological basis
of the low RS of young birds and the
decreased RS of newly-formed pairs of older
birds? Lehrman (1965) and Kunkel (1974)
suggested that LTPBs serve to promote
physiological synchrony between members
of a pair, but there is as yet no published
study on this point (but see Fowler (1993)
for a demonstration of LTPBs and physiological synchrony in Magellanic Penguins).
These questions remain to be answered, and
their answers will go far towards increasing
understanding of the mechanisms of age-
325
related RS, and how RS is maximized over
the life of an individual.
ACKNOWLEDGMENTS
This review is an outgrowth of my doctoral dissertation studies at the University
of Washington, Dept. of Zoology. The
development of the ideas presented here was
aided and abetted by discussions with many
individuals, but especially Lee Astheimer,
Tom Coombs-Hahn, Rachel Levin, and the
members of my dissertation committee:
Mike Beecher, Dee Boersma, Jim Kenagy,
Gordon Orians, Sievert Rohwer and John
Wingfield. Drafts of the manuscript were
criticized and improved by Steve Adolph
(who suggested Fig. 2), Fran Hanzawa and
Rachel Levin.
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ability in Adelie penguins. Auk 89:559-566.
Baeyens, G. 1981. Functional aspects of serial
monogamy: The magpie pair-bond in relation to
its territorial system. Ardea 69:145-166.
Baillie, S. R. and H. Milne. 1982. The influence of
age on breeding in the Eider Somateria mollisima.
Bird Study 29:55-66.
Beletsky, L. D. and G. H. Orians. 1989. Familiar
neighbors enhance breeding success in birds. Proc.
Nat. Acad. Sci. U.S.A. 86:7933-7936.
Blus, L. J. and J. A. Keahy. 1978. Variation in reproductivity in the brown pelican. Auk 95:128-134.
Bradley, J. S., R. D. Wooller, I. J. Skira, and D. L.
Serventy. 1990. The influence of mate retention
and divorce upon reproductive success in shorttailed shearwaters Puffinus tenuirostris. J. Anim.
Ecol. 59:487-496.
Bradley, J. S., R. E>. Wooller, and I. J. Skira. 1995.
The relationship of pair-bond formation and duration to reproductive success in short-tailed shearwaters Puffinus tenuirostris. J. Anim. Ecol. 64:31—
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