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10.1 Introduction
Life-history traits refl ect how individuals allocate
their time and energy to competing activities, such
as growth, maintenance, and reproduction ( Roff,
2002 ). The ability to adjust these traits is likely to
determine the response of populations to long-term
modifi cations of the environment, such as global cli-
mate change and habitat loss. Some populations
may be able to change quickly because individuals
show high levels of phenotypic plasticity, defi ned as
the ability of a single genotype to modify its pheno-
type under different environmental conditions
( Houston and McNamara, 1992 ; Pigliucci, 2001 ). In
terms of adjusting to climate change, phenotypic
plasticity in birds may involve changes in diet, habi-
tat selection, and migratory behaviour, but one of
the most studied aspects has been phenology or the
timing of breeding. Plasticity in the timing of breed-
ing appears to be relatively high in many songbirds
( Przybylo et al. , 2000 ; Brommer et al. , 2005 ; Nussey
et al. , 2005 ) because in different years some individu-
als may vary their breeding dates by almost a month
in response to local weather conditions ( Wesolowski
and Cholewa, 2009 ). Nonetheless, plasticity in
timing of reproduction can also be limited by devel-
opmental, hormonal ( Sockman et al. , 2006 ), genetic,
and evolutionary constraints. For example, the abil-
ity of migratory species to shift their breeding date
in response to climate change will be constrained if
the time of arrival on the breeding grounds from
wintering areas is infl exible because it is set by
photoperiod, rather than temperature or food
availability ( Both and Visser, 2001 ). Thus, a change
in the reliability of environmental cues can some-
times result in maladaptive behaviour (evolutionary
traps; Pulido and Berthold, 2004 ; Miner et al. , 2005 ).
Understanding the ecological and evolutionary
basis of plasticity in varying environments is neces-
sary for predicting the effects of climate change on
bird populations. However, at present, little is
known about the mechanisms and consequences of
plasticity for bird populations facing climate change
( Nussey et al. , 2007 ; Lyon et al. , 2008 ).
There is mounting evidence from long-term stud-
ies that birds are advancing their date of laying
associated with increasing mean temperatures
(see Appendix). Indeed, this is some of the strongest
evidence for the effects of climate change on wild
populations (see reviews by Walther et al. , 2002 ;
Parmesan and Yohe, 2003 ; Root et al. , 2003 ). Part of
this attention may simply refl ect the fact that laying
(or hatching) dates are some of the most easily gath-
ered and least biased measures of avian reproduc-
tion. However, timing of laying has profound effects
on overall breeding performance as there are often
strong genetic ( Garant et al. , 2008 ) and phenotypic
( Winkler and Allen, 1996 ; Mills et al. , 2008 ) cou-
plings between timing of breeding and clutch size,
which set a fi xed upper limit on overall reproduc-
tive success. Indeed, it is becoming increasingly
apparent that timing of breeding, number and size
of clutches, duration of parental care, and survival
are integrated and respond in a coordinated fashion
to environmental factors, particularly relative food
abundance ( Both and Visser, 2005 ; McNamara et al. ,
CHAPTER 10
Effects of climate change on timing of breeding and reproductive success in birds Peter O. Dunn and David W. Winkler
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2008 ). By advancing the timing of breeding, climate
change may also affect other aspects of reproduc-
tion such as the number ( Verboven et al. , 2001 ) and
size ( Both and Visser, 2005 ) of clutches, incubation
behaviour ( Cresswell and McCleery, 2003 ; Cooper
et al. , 2005 ), and recruitment ( Drent, 2006 ; Wilson et al. , 2007 ). Our review focuses primarily on timing of
breeding (laying or hatch dates) because this gener-
ally has a strong connection with clutch size and
subsequent reproductive success, but we also dis-
cuss the effects of climate on other reproductive
traits. We begin with a review of proximate factors
infl uencing laying date, summarize the causes and
rate of change in laying date, and then analyse how
climate change is infl uencing laying date at the
intra- and inter-specifi c levels.
10.2 What factors infl uence laying date?
Although most birds lay earlier when spring tem-
peratures are warmer ( Dunn, 2004 ), there are a vari-
ety of other proximate factors infl uencing the start
of breeding, including precipitation ( Skinner et al. , 1998 ; Leitner et al. , 2003 ; Rodriguez and Bustamante,
2003 ), food abundance, breeding density, and pho-
toperiod and hormones ( Dawson, 2008 ). For most
temperate-breeding birds, these factors are thought
to act in a hierarchy, starting with increasing
daylength (photoperiod) as the primary cue for
gonadal maturation and release of hormones in the
spring. In tropical species, it was previously thought
that daylength cues were too small to time breeding
seasons, but there is now evidence from tropical spe-
cies and experiments with temperate species show-
ing that small changes in daylength can initiate
reproduction (reviewed by Dawson, 2008 ). In more
unpredictable climates, such as those in deserts,
breeding appears to be more fl exible, depending on
favourable environmental conditions, particularly
the onset of rainfall ( Hau et al. , 2004 ). Although some
species such as zebra fi nches ( Taeniopygia guttata )
can breed at almost any time of year when food
becomes abundant, other opportunistic species,
such as crossbills ( Loxia spp.), appear to require reg-
ular changes in photoperiod to initiate a physiologi-
cal window during which breeding can occur once
food conditions are adequate ( Dawson, 2008 ).
Increasing photoperiod often initiates reproductive
activity in temperate birds, but species differ in
terms of the threshold amount of light required to
start gonadal growth, and they also differ in the rate
at which growth proceeds under increasing
daylength ( Dawson, 2008 ). Photoperiod is fi xed at
the same latitude, but these inter-specifi c differences
in gonadal responses could infl uence the rate at
which various species respond to other environmen-
tal conditions. The timing of breeding varies between
years, so there is clearly more than just photoperiod
regulating breeding, and it is likely that photoperiod
interacts simultaneously with other environmental
cues such as food abundance, temperature, and
social stimulation to set the physiological window
during which egg-laying will occur ( Dawson, 2008 ;
Schoech and Hahn, 2008 ).
Food abundance is thought to be one of the most
important of the secondary cues used to fi ne-tune
time of breeding. Females appear to time the laying
of their clutch such that hatching occurs near the
peak of food availability, when the energetic demands
of offspring are presumably the greatest ( Figure
10.1a ). However, food availability earlier in the sea-
son during egg-laying may also be important in some
species ( Perrins, 1970 ; Bryant, 1975 ), and other
aspects of life history, such as the number of broods
per season ( Crick et al. , 1993 ; Visser et al. , 2003 ), may
have an infl uence. In multi-brooded species, total
reproductive success for the season depends more on
the duration of the season than in single-brooded
species, so the timing of the fi rst brood relative to
peak food abundance is less important, and they
generally start breeding as soon as possible in the
spring ( Crick et al. , 1993 ). If climate change reduces
the period when food is available for second broods,
then the reproductive value of second broods declines
and fewer birds will produce second broods ( Visser
et al. , 2003 ; Husby et al. , 2009 ). These females, which
now only have a single brood, are expected to start
laying closer (relative to double-brooded females) to
the peak of insect abundance ( Visser et al. , 2003 ). This
appears to be occurring in great ( Parus major ) and
blue ( P. caeruleus ) tits, as populations that show a
larger decline in the proportion of second broods
also show a relatively small change in laying date
over time ( Visser et al. , 2003 ). In contrast, populations
that are primarily single brooded have shown larger
advancement in laying dates because a greater
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proportion of these females are adjusting their single
clutch to the time of peak food abundance, which is
generally advancing. Thus, single-brooded popula-
tions appear to be more sensitive to climate change
(see also Section 10.5 ). Note that across species, food
supplementation experiments suggest that multi-
brooded species advance their laying date more than
single-brooded species ( Svensson, 1995 ), which may
not seem consistent with the discussion above.
However, the timing of food supplements in these
experiments may not be similar to changes in food
abundance caused by climate change and thus the
results from experiments and unmanipulated birds
may not be directly comparable.
In addition to acting on lower trophic levels to
infl uence food abundance, temperature could also
have direct effects on thermoregulation of birds or
their ability to maintain viable eggs ( Stevenson and
Bryant, 2000 ). Thus, temperature could be an ener-
getic constraint on laying date and not just a cue for
breeding. Experiments that heat and cool aviaries
under controlled conditions ( Meijer et al. , 1999 ;
Salvante et al. , 2007 ; Visser et al. , 2009 ) also suggest
that there can be direct effects of temperature on
timing of laying. Furthermore, increasing tempera-
tures might select for smaller clutches if larger
clutches are currently maintained by the benefi ts of
reduced clutch cooling when females take breaks
from incubation ( Cooper et al. , 2005 ).
It is thought that climate change is making the
current cues for breeding (photoperiod, temperature,
and food) poorer predictors of food supply and,
hence, the optimal time for breeding. In other words,
the cues become decoupled from peaks in food abun-
dance, which will potentially lead to mismatches
between the start of breeding and the availability of
food for nestlings. For example, these mismatches
may occur when birds base their spring migration on
photoperiod and arrive ‘too late’ on the breeding
grounds to take advantage of a peak in food abun-
dance that has shifted earlier because of warmer
spring temperatures. These mismatches are thought
to arise in insectivorous birds because increased
spring temperatures lead to much faster develop-
ment of ectothermic insect prey than their own
homoeothermic nestlings. For example, the develop-
ment of winter moths can accelerate from 56 to 23
days ( Buse et al. , 1999 ). Thus, warmer spring temper-
atures can lead to earlier peaks in insect abundance
and, consequently, a mismatch between the timing of
peak food abundance and maximum food require-
ments of developing young ( Visser et al. , 1998 ).
The mismatch hypothesis is primarily applicable
to species in which the main selective force on tim-
ing of laying is synchronization between the food
supply and the peak energy demands of the off-
spring. Even though it has been over 50 years since
Lack (1954) proposed that parents time their
Figure 10.1 Mean date of laying in relation to the date of peak food abundance of (a) pied fl ycatchers and (b) tree swallows. Laying date was related to date of peak caterpillar abundance in a Dutch population of fl ycatchers (1985–2004, r = 0.82, n = 19, P < 0.001; Both and Visser, 2005 ), but it was not signifi cantly related to biomass of fl ying insects in two populations of tree swallows in North America (1986–2005, r = 0.17, n = 17 site-years, P = 0.31; Dunn et al. , in preparation). The lines are the linear regression lines. Panel (a) reprinted with the permission of Wiley-Blackwell.
50(a)
45
40
35
40
Mea
n la
ying
dat
e (d
ays)
50Caterpillar peak date (days)
60 70
30(b)
25
20
15
0 10
Mea
n la
ying
dat
e
Flying insect peak date(1=1 May)
20 30 40 50
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breeding to coincide with seasonal peaks of food
abundance, there have been relatively few studies
with direct measurements of natural food abun-
dance in relation to timing of breeding. In contrast
to Lack’s hypothesis, several studies indicate that
laying date is not timed to match a peak in food
abundance later in the season when offspring
demands are greatest. For example, reed warblers
Acrocephalus scirpaceus feed on insects that are abun-
dant throughout the season and there is no clear
peak in abundance ( Halupka et al. , 2008 ). Similarly,
in tree swallows Tachycineta bicolor , food remains
abundant long after chicks fl edge (Winkler, in prep-
aration), and temperatures and insect abundance
are highly variable prior to laying and do not pro-
vide reliable cues to food abundance during the
nestling period ( Figure 10.1b , Dunn et al. , in prepa-
ration). In other species, such as waterfowl, timing
of laying also appears to have little infl uence on the
number of fl edglings because success is most
strongly infl uenced by nest predation ( Drever and
Clark, 2007 ; but see Brinkhof et al. , 1997 ).
The absolute abundance of food and its distribu-
tion throughout the breeding season may also affect
reproductive success in addition to its timing. For
example, Durant et al. (2005) showed that chick sur-
vival in Atlantic puffi ns Fratercula arctica was only
related to the abundance of herring Clupea harengus ,
their main food, and not to the degree of mismatch
between the average hatch date and the date of her-
ring arrival. Thus, abundant food resources may
compensate for mismatches in timing. The effect of
mismatches is also thought to depend on the length
of time food is available and other aspects of life
history such as adult mortality. In a theoretical
model for migratory species, Jonzén et al. (2007)
predicted that advances in laying date will be
weaker when food for nestlings is available for a
longer period of time. In general, longer availability
of food will reduce the risk of breeding failure and
adult mortality and allow a wider range of breeding
times. For example, in pied fl ycatchers, birds have
not changed their arrival date on the breeding
grounds ( Both and Visser, 2001 ) , which is consistent
with theory, if the mortality risk to adults is moder-
ate and there is strong competition to arrive early
and gain access to limited nest sites. However,
any change in adult mortality (higher or lower) is
predicted to lead to shifts in the optimal arrival
date. Timing of breeding can also respond to adult
mortality rates during the breeding season, with
earlier breeding being selected if the risk of adult
mortality later in the season is not negligible ( Goutis
and Winkler, 1992 ). Thus, accurate predictions
about the impact of climate change on breeding
dates may require information about the size and
shape of the distribution of food, as well as patterns
of adult mortality throughout the season.
Understanding the ecological and physiological
mechanisms behind the decision to breed will be
increasingly important in the future as tempera-
tures are predicted to increase dramatically, and at
these higher temperatures we may fi nd that there
are thresholds or other non-linearities that dramati-
cally alter the relationships between temperature,
resources, and breeding decisions ( Stenseth and
Mysterud, 2002 ; Lyon et al. , 2008 ). For example,
some North American tree species are predicted to
advance their date of leaf unfolding for the fi rst half
of this century, but later, when temperatures are
higher, they are expected to show delays and abnor-
mal unfolding ( Morin et al. , 2009 ). These delays are
also predicted to be stronger in the southern USA,
where warmer temperatures will produce a lack of
the chilling temperatures necessary to break bud
dormancy. Non-linear responses to climate could
also occur if there are some cohorts of birds that
respond differently because of previous experience
or conditions at birth that affect their plasticity to
temperature ( Wilson et al. , 2007 ).
10.3 What are the causes of changes in laying date?
Inferences about the causes of change in timing of
breeding have to be made cautiously because most
studies are based on correlations between breeding
date and temperature or other climate variables
(North Atlantic oscillation, NAO; precipitation).
Thus, analyses could be confounded by changes in
human land use, pollution, or changes in breeding
density. For example, if habitat changes lead to
smaller populations and lower breeding density,
then there might be more resources available for each
individual, which could reduce competition and
allow individuals to shift to an earlier breeding date.
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Changes in population size are known to bias esti-
mates of fi rst arrival dates ( Tryjanowski et al. , 2005 ;
Miller-Rushing et al. , 2008 ), so they may also bias
estimates of the earliest date of egg-laying. In a
Scottish seabird colony, common guillemots Uria aalge are increasing in numbers and laying eggs later
( Frederiksen et al. , 2004 ), as might be predicted if
intra-specifi c competition affects the timing of repro-
duction. However, in the same breeding colony,
black-legged kittiwakes Rissa tridactyla are laying
eggs later and declining in numbers, so laying dates
may also be infl uenced by factors such as social stim-
ulation and individual experience ( Frederiksen et al. , 2004 , personal communication). The effects of
changes in population density and habitat quality
have rarely been addressed, but might be discounted
if the study is conducted in a pristine area where
anthropogenic effects on breeding conditions are
lacking (e.g. Wesolowski and Cholewa, 2009 ) or if
researchers test for effects of density on laying date
( Dunn and Winkler, 1999 ; Sanz et al. , 2003 ; Dyrcz and
Halupka, 2009 ; Wanless et al. , 2009 ).
At the population level, timing of breeding can
change because of phenotypic plasticity, demo-
graphic shifts, or natural selection (micro-evolu-
tionary change). Phenotypic plasticity should
produce changes most readily, and if for any reason
the range of change allowed by plasticity is
exceeded, then evolutionary changes should occur
( Bradshaw and Holzapfel, 2006 ; Visser, 2008 ).
Indeed, the great majority of studies reviewed in
Table 10.1 are consistent with a phenotypically plas-
tic response, and approximately half of the studies
have found evidence for selection on laying date
(i.e. signifi cantly greater reproductive success for
earlier nesting individuals), including great tits
( Visser et al. , 1998 ), pied fl ycatchers ( Both and Visser,
2001 ), barnacle geese Branta leucopsis van der Jeugd
et al. , 2009 ), thick-billed murres Uria lomvia Gaston
et al. , 2009 ), and common guillemots ( Reed et al. , 2009 ). Several other studies explicitly searched
without success for signifi cant selection coeffi cients
or correlations between breeding success and lay-
ing date, including great tits in the UK ( Cresswell
and McCleery, 2003 ), ducks in Saskatchewan
( Drever and Clark, 2007 ), kittiwakes and guillemots
in Scotland ( Frederiksen et al. , 2004 ), and collared
fl ycatchers in Sweden Ficedula albicollis Sheldon
et al. , 2003 ). Ultimately, we might expect climate-
related selection to produce a micro-evolutionary
change in phenology, but only a few studies have
actually shown this to date, which may be partly
due to the diffi cultly in collecting long-term pedi-
gree-based data on wild populations (see Visser,
2008 for a review). Much of this lack of evidence for
micro-evolutionary change may be due to the fact
that the range of phenotypic plasticity has not been
exceeded (e.g. Charmantier et al. , 2008 ).
Recent work on non-migratory great tits in
England ( Charmantier et al. , 2008 ) and The
Netherlands ( Nussey et al. , 2005 ) has highlighted
differences between these populations in their
responses to temperature: the British tits seem to be
keeping up with changes in temperature and their
prey and their population size is increasing, whereas
many of the Dutch birds are lagging behind and
average fi tness is declining. One promising hypoth-
esis to explain these differences is that the birds are
responding to different cues in determining when
to begin laying ( Lyon et al. , 2008 ). Have the correla-
tions between cues and environments for some rea-
son been less reliable in The Netherlands in the past,
selecting for a greater reliance on photoperiodic
cues? Or is there something different in the way
that they respond to temperature and photoperiod
that may arise from other selective pressures (cf.
Silverin et al. , 2008 )? One contributing factor to
these differences may be greater isolation of the tit
population in Great Britain compared with the
mainland population in The Netherlands. Greater
gene fl ow on the mainland may have reduced the
rate of local adaptation in the Dutch population,
leading to non-optimal timing of breeding, similar
to the non-optimal clutch sizes reported in Belgian
tits ( Dhondt et al ., 1990 ). In migratory species, such
as barn swallows Hirundo rustica and pied fl ycatch-
ers, there is evidence that some of these geographic
differences in arrival or breeding times may arise, at
least partially, from the different environmental
conditions that they experience in different parts of
the winter range in Africa or along migration routes
( Both et al. , 2006 ; Balbontín et al. , 2009 ).
There is also reason for caution in interpreting
potential mismatches between the phenologies of
breeding birds and their prey. Although there is
good evidence from a few detailed studies that
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populations are not responding to temperature
changes at the same rate as their food supply ( Both
et al. , 2009 ), it is not always clear what the conse-
quences are for the populations. Most mismatch
interpretations have at least implicitly assumed a
sharp peak in the summer food availability for
growing chicks, a peak that, if missed, has serious
repercussions for offspring production. Very few
studies, however, have measured the food supply
directly, and at least some species have food avail-
able for a long period in the summer ( Halupka
et al. , 2008 ; Winkler, in preparation), thus reducing
the impacts of differential phenological shifts in
birds and their prey. Extended periods of food
availability probably represent successive availa-
bility of several different insect species, and Winkler
et al. (2002) suggested that birds with greater diet
diversity will be less impacted by phenological
shifts in prey. Even in such species with a broad
summer plateau of food availability, however, there
is the potential for a mismatch, as the entire sum-
mer insect fauna might shift earlier, leaving a gap
in late summer and autumn that may hit fl edglings
hard during the diffi cult post-fl edging transition to
independence and may hit all age classes prepar-
ing for migration.
Even when there are mismatches, it is not always
clear that they are detrimental to population growth.
In Sweden, barnacle geese young hatch several
weeks after the peak in forage quality (nitrogen con-
tent), and this has produced stronger selection for
earlier breeding, but, despite the mismatch, this
population produces more surviving young than an
arctic Russian population whose young hatch near
the peak in forage quality ( van der Jeugd et al. , 2009 ).
This example shows that we also need to consider
other possible adjustments of the breeding cycle to
climate change, such as changes in the number of
broods, the amount of parental care, or post-fl edging
survival which could compensate. Thus, it is impor-
tant to differentiate between what Winkler et al . (2002) called the adaptive and demographic effects
of phenological shifts. We may sometimes think that
birds would be better adapted doing things differ-
ently (adaptive effects), but if that different behav-
iour is not refl ected in different population sizes or
dynamics (demographic effects), then the distinc-
tion may not be important for conservation.
10.4 Laying date is advancing in most species
Evidence for long-term changes in the phenology
of birds is accumulating rapidly from around the
world. Long-term studies of the date of laying (or
hatching) have been conducted in at least 68 species
(mean = 42 years of data; Table 10.1). One of the old-
est continuous records of laying started in 1897 in
The Netherlands, where eggs of northern lapwings
Vanellus vanellus are harvested for human consump-
tion, and newspapers record the fi rst egg each
spring, which is given to the Queen ( Both et al. , 2005 ). Some of the largest of these studies have used
nest records contributed by volunteers over many
years in the UK ( Crick and Sparks, 1999 ) and North
America ( Dunn and Winkler, 1999 ; Torti and Dunn,
2005 ), but there are still just a handful of these large-
scale studies. Most reported studies (84%, 31/37)
have been long-term projects at a single site on a
single species (Table 10.1).
Over the years, there has been a signifi cant
advance in laying date of 59% (40/68) of species,
and 79% (53/67) of species lay earlier during warmer
years, in at least one study (Table 10.1). Based on
current estimates, birds are advancing their laying
dates by an average of 0.13 days per year (±0.03 SE,
n = 52 species, range: −0.80 to 0.51), and they are lay-
ing 2.40 (±0.27 SE) days earlier for every degree cen-
tigrade warmer ( n = 52 species, range: −10.3 to −0.01;
Table 10.1). Given projections for future global
warming of up to 4 °C ( Intergovernmental Panel on
Climate Change, 2007 ), we might expect birds to be
laying approximately 15 days earlier by the end of
this century. Thus, it seems likely that even those
species that have not yet responded to climate
change will eventually show advancement in timing
of breeding. However, the magnitude of these
changes and their impacts are still unclear.
10.5 Inter-specifi c variation in laying date
Although birds are generally breeding earlier, there
is a great deal of variation between and within spe-
cies that is not well understood. Some topics that
are particularly important are (1) the ability of dif-
ferent species to adjust their phenology to that of
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the resources they need for breeding (e.g. the degree
of mismatch between bird populations and their
food supply) and (2) the causes of geographic vari-
ation within species, because this will indicate
how much particular species can change and the
causes (phenotypic or evolutionary) of intra-specifi c
variation.
Comparative evidence indicates that, overall, bird
species are keeping pace with changes in the phenol-
ogy of lower trophic levels, which suggests that mis-
matches are uncommon. The rate of change (mean ±
SE days per decade) in avian laying dates (−3.77 ±
0.70, n = 41 species) does not appear to be different
from that of changes in phenology of trees (−3.3 ±
0.87), shrubs (−1.1 ± 0.68), or butterfl ies (−3.7 ± 0.78;
Parmesan, 2007 ). On a per-year basis, this rate of
advancement in birds (0.37 day/year) is greater than
our estimate (0.13 day/year) in Table 10.1, but it was
based on older data ( Root et al. , 2003 ; Parmesan and
Yohe, 2003 ) from a variety of different estimates of
timing of arrival and breeding, not just laying dates.
Studies of trophic interactions at the same location
are less likely to be biased by sampling differences
and here there is more evidence for mismatches.
Indeed, several studies have found mismatches or
differences between the responses of trophic levels to
climate ( plankton: Edwards and Richardson (2004) ;
plant and insects in a grassland: Voigt et al. (2003) ;
reviewed by Visser and Both ( 2005 ) ).
Species may vary in their response to climate
change for a variety of ecological, life history, geo-
graphic, and phylogenetic reasons. In particular,
migratory species may have a different hierarchy of
cues for breeding (e.g. photoperiod and food) than
resident species. There could also be differences in
geography (temperate vs. tropical) that affect the
magnitude of response, as there have been much
larger increases in temperature in certain regions,
particularly above 50 °N ( Myneni et al. , 1997 ). Indeed,
across a variety of taxa, there has been a small but
signifi cantly greater response at higher latitudes
( Parmesan, 2007 ). Thus, we might predict greater
phenological responses by birds at higher latitudes.
Analysis of the 52 species with long-term data on
changes in laying date (Table 10.1) revealed that
species that typically have a single brood advanced
their laying date about three times faster than spe-
cies with two or more broods per season (−0.19 vs.
−0.06 days per year; t 50
= 2.0, P = 0.046), as predicted
in Section 10.2 . Thus, it appears that single-brooded
species are responding more rapidly to climate
change, as Visser et al. (2003) found in blue and
great tits (see also Husby et al. , 2009 ). The response
of birds to climate change may also vary across spe-
cies if there are differences in how various types of
food respond to changes in air temperature. For
example, we might expect insects and plants to
respond more rapidly than vertebrates and thus
increase the response of birds that feed on these
groups. However, herbivorous (−0.45 ± 0.15 day/
year, n = 2) and insectivorous (−0.11 ± 0.03, n = 43)
species advanced their laying dates at rates not sig-
nifi cantly different from species that feed on verte-
brates, primarily fi sh (−0.14 ± 0.15 day/year, n = 7,
F 2,49
= 2.2, P = 0.12). Note that very few studies have
been published on herbivorous and vertebrate-
eating species. Future analyses should also consider
the spatial scale at which species forage and dis-
perse. For example, even within the same region,
different species of seabirds that rely on similar
types of prey can respond differently depending on
where they acquire their food (i.e. offshore or
inshore; Frederiksen et al. , 2004 ).
If temperature has a direct effect on thermoregula-
tion and energy balance, then we might also expect
the body size of birds to infl uence their response to
climate change. Using the data of Crick and Sparks
(1999) , Stevenson and Bryant (2000) found that the
long-term change in laying date was smallest in large
species and greatest in small species. However, we
found no effect of body mass in our analysis with
almost twice as many species included in the data set
( r 2 < 0.001, F 1,49
= 0.004, P = 0.95). Obviously, more spe-
cies need to be examined, particularly large-bodied
predators, which have not yet been studied as exten-
sively. Additional analyses showed that migratory
behaviour, coloniality (yes/no), and continent had no
signifi cant effect on the advancement of laying (Dunn,
unpublished data).
10.6 Intra-specifi c differences in the timing of breeding
Within species, there is substantial geographic vari-
ation in the response of species to climate change.
Although global temperatures have increased an
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120 E F F E C T S O F C L I M AT E C H A N G E O N B I R D S
average of 0.6 °C, there have been much larger
increases in certain regions, particularly above 50°N
( Myneni et al. , 1997 ). Given that 94% of species breed
earlier in warmer springs, the most likely explana-
tion for the geographic differences in the timing of
breeding is local variation in temperature change. In
some well-studied species, such as pied fl ycatchers
( Both et al. , 2004 ), great and blue tits (e.g., Visser et al. , 2003 ; see also Sæther et al. , 2003 ), and barn swal-
lows ( Møller, 2008 ), there is considerable variation
among study sites that is related to local tempera-
ture differences. Similar geographic variation in the
response of species has also been reported in several
North American species, including tree swallows
( Dunn and Winkler, 1999 ; Hussell, 2003 ), killdeer
Charadrius vociferus , American robins Turdus migrato-rius , and eastern bluebirds Sialia sialis Torti and
Dunn, 2005 ). In particular, killdeer, American robins,
and eastern bluebirds showed a steeper negative
relationship between laying date and temperature at
more northerly locations ( Torti and Dunn, 2005 ),
while climate change had a stronger effect on laying
date at more western locations within the range of
tree swallows. Even large-scale climate indices such
as the NAO can have effects that differ geographi-
cally. In an analysis of 13 species of seabirds, the
NAO had a positive effect on breeding success in the
south, but a negative effect in the north ( Sandvik et al. , 2008 ). The strength of climate change may vary,
depending on the location and time period studied,
and its effects on avian phenology should be tested
whenever possible by including local-scale meteoro-
logical variables in the analysis.
Local differences in plant phenology may also
produce some ‘early’ sites at a micro-geographic
scale, and over time individuals could shift to these
earlier sites, resulting in advances in the mean lay-
ing date for the entire population ( Møller, 2008 ).
Gienapp and Visser (2006) also found that female
great tits in two nearby populations responded dif-
ferently to artifi cial peaks in food abundance. Even
within the same breeding location, the responses of
species may differ depending on the particular time
periods that they are sensitive to temperatures. For
example, based on a large-scale model ( Both and te
Marvelde, 2007 ), starlings Sturnus vulgaris are pre-
dicted to be advancing their laying date across
Europe, but pied fl ycatchers are expected to advance
their laying dates in western and central Europe
and delay laying in northern Europe. These differ-
ences between and within species are expected
because starlings lay eggs 25 days earlier than pied
fl ycatchers and temperatures are changing differ-
ently during these two time periods. Furthermore,
breeding time temperatures for pied fl ycatchers are
increasing in most of Europe (<60 °N) and decreas-
ing at more northerly breeding locations ( Both and
te Marvelde, 2007 ). Thus, intra-specifi c differences
in the response to climate change are common and
are mostly likely caused by geographic differences
in the extent and timing of warming.
10.7 How does timing of breeding relate to breeding performance?
In most species, especially those that rear only one
brood per season, individuals that start to lay earlier
also have larger clutch sizes, and this often translates
into more young fl edged. Given that many species
show a long-term advancement in laying date, we
might also expect an increase in clutch size in these
species, and possibly greater reproductive success.
However, the results are much more complicated.
Long-term advancement of laying and larger
clutches have been reported in some populations of
pied fl ycatchers ( Järvinen, 1989 , Winkel and Hudde,
1997 ) and fi rst broods of barn swallows ( Møller,
2002 ), but not in collared fl ycatchers ( Sheldon et al. , 2003 ), great or blue tits ( Winkel and Hudde, 1997 ),
tree swallows ( Winkler et al. , 2002 ), eastern bluebirds
( Torti and Dunn, 2005 ), or red-winged blackbirds
Agelaius phoeniceus ( Torti and Dunn, 2005 ).
It is not clear why clutch size has not increased in
populations with a shift towards earlier laying, but
there are a number of possible ecological explana-
tions. First, it may be that because of potential mis-
matches with the peak of food abundance for
nestlings (or a general decline in fl edgling survival)
the date of laying has a greater effect on reproduc-
tive success than laying a few additional eggs,
which will delay hatching. In pied fl ycatchers, for
example, the probability of recruitment declined
more strongly with hatch date in warmer years
when birds generally laid earlier ( Both and Visser,
2005 ). Thus, there was stronger selection against
relatively larger (and later) clutches; part of this
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T I M I N G O F B R E E D I N G A N D R E P R O D U C T I V E S U C C E S S 121
selection might come in the form of countervailing
survival selection on adults (i.e. larger clutches
reduce adult survival). In collared fl ycatchers,
Sheldon et al. (2003) suggested that there was strong
directional selection on the phenotype for earlier
laying, but an evolutionary response was prevented
by a countervailing trade-off with adult survival. A
similar type of trade-off with adult survival might
occur in populations that advance laying date but
show no change in clutch size. One problem with
this interpretation is that there is little evidence for
adult survival costs that are dependent on fecun-
dity (e.g. in tree swallows; Shutler et al. , 2006 ).
Second, there could be shifts in laying dates, but
no change in mean clutch size, if there are demo-
graphic changes that lead to earlier breeding by a
greater proportion of lower-quality individuals
(e.g. younger females) that lay smaller clutches
( Winkler et al. , 2002 ). A third possibility is that in
warmer years it is easier for all individuals to start
laying earlier, but this does not lead to any change
in how many eggs they lay because there is a shift in
the relationship between clutch size and laying date
without any change in slope. In this ‘relative’ model
of clutch size determination ( Winkler et al. , 2002 ),
the intercept of the regression line between clutch
size and laying date decreases in a warmer year, but
the slope stays the same ( Figure 10.2 ). In other
words, the line shifts to the left (earlier), so an ear-
lier laying date results in a similar clutch size. This
is a type of non-continuous response to climate
change, as there is a new relationship between
clutch size and laying date. In contrast, bird popula-
tions that follow the ‘absolute’ model move up (and
down) the same regression line each year, so when
spring is warmer and laying is earlier, the average
clutch size increases ( Figure 10.2 ). This would be a
continuous response, as the relationship between
clutch size and laying date is fundamentally the
same. In at least some species, there appears to be
strong selection to breed as early as possible because
it leads to acquiring a higher quality mate
(e.g. Kirkpatrick and Arnold, 1990 ) or because the
risk of mortality favours breeding as soon as condi-
tions allow ( Goutis and Winkler, 1992 ). Such selec-
tive forces raise the possibility that birds may
sometimes be laying eggs at a time when their
chicks hatch before the seasonal peak in food abun-
dance, and they suggest the possibility that the tim-
ing of laying is adapted to other factors besides the
timing of food supply for the chicks. These selective
forces also provide a rationale for the often-ob-
served correlation between laying date and other
aspects of individual quality (e.g. Bowlin and
Winkler, 2004 ). To date, most studies have found
that birds are laying earlier but not changing clutch
size; however, it is possible that further increases in
temperature will eventually lead to a change in
clutch size and breeding performance.
10.8 Conclusions and future avenues of research
There has been a tremendous increase in the number
of long-term studies of avian phenology in the last 5
years, more than doubling since an earlier review
( Dunn, 2004 ). Despite this increased interest and
Absolute model
Relative model
Lay date
Clu
tch
size
Clu
tch
size
Figure 10.2 Two different models of how birds respond to interannual changes in laying date from Winkler et al. (2002) . In the absolute model (top panel), the mean annual clutch size increases as laying date becomes earlier. However, in the relative model (bottom panel) earlier laying may result in a shift to a different (dashed) line and, as a consequence, no change in the mean clutch size.
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122 E F F E C T S O F C L I M AT E C H A N G E O N B I R D S
information, there are still many of the same needs for
additional data. Most importantly, we need a better
understanding of avian responses at a broader geo-
graphic scale. Most of our research has been limited
to single study sites, and we need to work collabora-
tively to broaden the scope (and relevance) of our
results. Groups of researchers are already organized
in Europe around some model species (e.g. Visser
et al. , 2003 ; Both et al. , 2004 ), but these large-scale
networks are just starting in North America, for
example, among researchers studying Tachycineta
swallows (www.golondrinas.cornell.edu/). A large-
scale national phenology network has started in the
USA (www.usanpn.org/), but, to date, it has focused
on plant phenology and it will only start collecting
information on animals in 2010. Networks of research-
ers are needed to increase the scope and sample sizes
required for studying responses to large-scale phe-
nomena such as climate change. Our review shows
that there is large variation in the response to climate
change within and among species. Understanding
this variation is critical if we aim to predict how bird
populations will respond to further temperature
increases. To date, the main contributions of pheno-
logical observations of birds have been monitoring
(i.e. how much bird populations are changing) and
detailed studies of changes in selection on laying date
(e.g. mismatches). In the future, we need to be able to
link these observations at broad geographic scales to
population trends of birds, as well as interactions
with other trophic levels. We still have a rudimentary
understanding of how temperature affects the food
supply and breeding performance of birds, primarily
because most researchers do not measure food abun-
dance. Much of our understanding of avian responses
to climate change comes from a handful of well-stud-
ied passerines that live in forests and feed on caterpil-
lars. Although these studies have been fundamental
in developing a mechanistic and theoretical under-
standing of how reproductive decisions of birds are
infl uenced by their food supply, their applicability to
other systems with different types and distributions
of food, such as waterfowl ( Drever and Clark, 2007 ),
aerial and aquatic insectivores ( Winkler et al. , 2002 ;
Halupka et al. , 2008 ; Pearce-Higgins et al. , 2009 ), rap-
tors ( Nielsen and Møller, 2006 ; Both et al. , 2009 ), and
seabirds ( Wanless et al. , 2009 ), may be limited. In the
future, the food supplies of many species are likely to
show non-linear responses to climate change, as a
consequence of disruptions at lower trophic levels.
For example, the phenology of some common tree
species (e.g. Populus spp.) is expected to advance and
then delay over the next century ( Morin et al. , 2009 ),
and differences in the tolerance of various trophic lev-
els to temperature may disrupt entire insect commu-
nities ( Voigt et al. , 2003 ), so we cannot assume a simple
linear relationship based on current patterns. There
are also likely to be major changes in Antarctic sea ice
availability that will have profound changes on the
entire marine community, reaching up to top preda-
tors such as penguins, but even here some species are
declining and others increasing ( McClintock et al. , 2008 ). Understanding the mechanistic relationships
between temperature, food supply, and avian breed-
ing performance, as well as the physiological basis for
these relationships, should be top priorities because
they are necessary for linking the responses of birds
to general circulation models of climate and predict-
ing long-term changes in populations. Ultimately,
however, we need to examine the entire life cycle of
species, as climate and other factors can sometimes
have larger effects on avian populations outside the
breeding season (e.g. Rolland et al. , 2008 ; Pearce-
Higgins et al. , 2009 ).
10.9 Acknowledgements
We thank M. Frederiksen, A.P. Møller, L.A. Whittingham,
and a reviewer for comments that improved the
manuscript.
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OUP CORRECTED PROOF – FINALS, 07/03/2010, SPi
Tabl
e 10
.1
Chan
ge in
layin
g da
tes
of 6
8 sp
ecie
s of
bird
s fro
m lo
ng-te
rm s
tudi
es.
Com
mon
nam
e Sp
ecie
s N
yea
rs
Layd
ate
chan
ge/y
ear
Layd
ate
chan
ge/°
C N
bro
ods
Sour
ces
Spar
row
haw
k Ac
cipite
r nisu
s 20
−
0.65
*
1 N
ielse
n an
d M
ølle
r (20
06)
Gre
at re
ed w
arbl
er
Acro
ceph
alus
aru
ndin
aceu
s 33
−
0.55
*
* 1
Halu
pka
et a
l . (2
008)
, Dyr
cz a
nd H
alup
ka (2
009)
Sedg
e w
arbl
er
Acro
ceph
alus
sch
oeno
baen
us
56
–2.0
4 *
2 Cr
ick a
nd S
park
s (1
999)
Eura
sian
reed
war
bler
Ac
roce
phal
us s
cirpa
ceus
56
−
0.48
*
−1.
24
* 1
Crick
and
Spa
rks
(199
9)
Long
-taile
d tit
Ae
gith
alos
cau
datu
s 56
0.
05
* −
5.51
*
1 Cr
ick a
nd S
park
s (1
999)
Red-
win
ged
blac
kbird
Ag
elai
us p
hoen
iceus
30
−
0.15
*
−1.
02
* 1
Torti
and
Dun
n (2
005)
, P. D
unn
(unp
ublis
hed
data
)
Mea
dow
pip
it An
thus
pra
tens
is 46
−
3.93
*
2 Cr
ick a
nd S
park
s (1
999)
Mex
ican
jay
Apeh
loco
ma
ultra
mar
ina
28
−0.
38
* −
0.40
*
1 Br
own
et a
l. (1
999)
Swift
Ap
us a
pus
25
−0.
20
* −
0.95
1
Rubo
lini e
t al.
(200
7)
Barn
acle
gee
se
Bran
ta le
ucop
sis
24
−0.
30
* −
0.02
*
1 va
n de
r Jeu
gd e
t al.
(200
9)
Linn
et
Card
uelis
can
nabi
na
57
0.12
*
−2.
92
* 2
Crick
and
Spa
rks
(199
9)
Gre
enfi n
ch
Card
uelis
chl
oris
57
0.04
*
−3.
73
* 2
Crick
and
Spa
rks
(199
9)
Ring
ed p
love
r Ch
arad
rius
hiat
icula
52
−
1.09
*
2 Cr
ick a
nd S
park
s (1
999)
Killd
eer
Char
adriu
s vo
cifer
ous
37
−0.
08
−1.
83
* 2
Torti
and
Dun
n (2
005)
, P. D
unn
(unp
ublis
hed
data
)
Whi
te-th
roat
ed d
ippe
r Ci
nclu
s cin
clus
53
0.15
*
−1.
59
* 2
Crick
and
Spa
rks
(199
9)
Carri
on c
row
Co
rvus
cor
one
57
−0.
32
* 1
Crick
and
Spa
rks
(199
9)
Yello
wha
mm
er
Embe
riza
citrin
ella
57
2
Crick
and
Spa
rks
(199
9)
Reed
bun
ting
Embe
riza
scho
enicl
us
53
−2.
64
* 2
Crick
and
Spa
rks
(199
9)
Euro
pean
robi
n Er
ithac
us ru
becu
la
57
−3.
51
* 2
Crick
and
Spa
rks
(199
9)
Littl
e pe
ngui
n Eu
dypt
ula
min
or
21
0.03
−
0.77
*
1 Ch
ambe
rs (2
004)
, Cul
len
et a
l. (2
009)
Colla
red
fl yca
tche
r Fi
cedu
la a
lbico
llis
22.7
−
0.30
*
−1.
32
* 1
Both
et a
l. (2
004)
, Wei
ding
er a
nd K
rál (
2007
)
Pied
fl yc
atch
er
Fice
dula
hyp
oleu
ca
21.5
−
0.15
*
−1.
51
* 1
Laak
sone
n et
al.
(200
6), B
oth
et a
l. (2
004)
Tufte
d pu
ffi n
Frat
ercu
la c
irrha
ta
28
−0.
80
* *
1 G
jerd
rum
et a
l. (2
003)
Chaf
fi nch
Fr
ingi
lla c
oele
bs
57
−0.
07
* −
4.42
*
2 Cr
ick a
nd S
park
s (1
999)
Amer
ican
coot
Fu
lica
amer
icana
28
0.
25
−0.
68
2 To
rti a
nd D
unn
(200
5), P
. Dun
n (u
npub
lishe
d da
ta)
Com
mon
moo
rhen
G
allin
ula
chlo
ropu
s 34
Cr
ick a
nd S
park
s (1
999)
Aust
ralia
n m
agpi
e G
ymno
rhin
a tib
icen
21
* −
0.08
*
1 G
ibbs
(200
7)
Eura
sian
oyst
erca
tche
r Ha
emat
opus
ost
rale
gus
34
0.03
*
1 Cr
ick a
nd S
park
s (1
999)
Barn
sw
allo
w
Hiru
ndo
rust
ica
29.5
−
0.15
*
−2.
09
2 Cr
ick a
nd S
park
s (1
999)
, Rub
olin
i et a
l. (2
007)
,
Nie
lsen
and
Møl
ler (
2006
), M
ølle
r (20
08)
Whi
te-ta
iled
ptar
mig
an
Lago
pus
leuc
urus
25
−
0.60
*
−2.
32
* 1
Wan
g et
al.
(200
2)
Com
mon
gul
l La
rus
canu
s 37
0.
02
−1.
43
* 1
Brom
mer
et a
l. (2
008)
Song
spa
rrow
M
elos
piza
mel
odia
32
−
0.28
−
0.28
2
Torti
and
Dun
n (2
005)
, P. D
unn
(unp
ublis
hed
data
)
Pied
wag
tail
Mot
acill
a al
ba
57
−0.
75
* 2
Crick
and
Spa
rks
(199
9)
Gre
y w
agta
il M
otac
illa
ciner
ea
47
Crick
and
Spa
rks
(199
9)
Spot
ted
fl yca
tche
r M
uscic
apa
stria
ta
57
0.11
*
−2.
72
* 2
Crick
and
Spa
rks
(199
9)
OUP CORRECTED PROOF – FINALS, 07/03/2010, SPi
Com
mon
nam
e Sp
ecie
s N
yea
rs
Layd
ate
chan
ge/y
ear
Layd
ate
chan
ge/°
C N
bro
ods
Sour
ces
Blue
tit
Paru
s ca
erul
eus
27
–0.3
4 *
−2.
62
* 2
Win
kel a
nd H
udde
(199
7), V
isser
et a
l. (2
003)
,
Dole
nec
(200
7), W
esol
owsk
i and
Cho
lew
a (2
009)
Gre
at ti
t Pa
rus
maj
or
29
−0.
29
* −
2.50
*
2 W
inke
l and
Hud
de (1
997)
, Viss
er e
t al.
(200
3), N
ielse
n
and
Møl
ler (2
006)
, Wes
olow
ski a
nd C
holew
a (2
009)
Mar
sh ti
t Pa
rus
palu
stris
27
−
0.16
−
1.97
*
1 Do
lene
c (2
006)
, Wes
olow
ski a
nd C
hole
wa
(200
9)
Hous
e sp
arro
w
Pass
er d
omes
ticus
25
−
0.19
−
1.69
2
Nie
lsen
and
Møl
ler (
2006
), Ru
bolin
i et a
l. (2
007)
Tree
spa
rrow
Pa
sser
mon
tanu
s 54
−
0.03
*
−4.
83
* 2
Crick
and
Spa
rks
(199
9), N
ielse
n an
d M
ølle
r (20
06)
Euro
pean
sha
g Ph
alac
roco
rax
arist
otel
is 17
−
0.23
−
10.3
0 *
1 Fr
eder
ikse
n et
al.
(200
4)
Com
mon
reds
tart
Phoe
nicu
rus
phoe
nicu
rus
55
−0.
18
* −
1.11
*
2 Cr
ick a
nd S
park
s (1
999)
Chiff
chaf
f Ph
yllos
copu
s co
llybi
ta
59
−0.
17
* −
3.98
*
2 Cr
ick a
nd S
park
s (1
999)
Woo
d w
arbl
er
Phyll
osco
pus
sibila
trix
55
−0.
20
* −
1.93
*
1 Cr
ick a
nd S
park
s (1
999)
Will
ow w
arbl
er
Phyll
osco
pus
troch
ilus
57
0.02
*
−1.
47
* 2
Crick
and
Spa
rks
(199
9)
Blac
k-bi
lled
mag
pie
Pica
pica
54
−
0.11
*
1 Cr
ick a
nd S
park
s (1
999)
Red-
cock
aded
woo
dpec
ker
Pico
ides
bor
ealis
19
−
0.20
*
* 1
Schi
egg
et a
l. (2
002)
Dunn
ock
Prun
ella
mod
ular
is 57
−
0.16
*
−2.
33
* 2
Crick
and
Spa
rks
(199
9)
Bullfi
nch
Py
rrhul
a py
rrhul
a 57
−
6.98
*
2 Cr
ick a
nd S
park
s (1
999)
Blac
k-le
gged
kitt
iwak
e Ri
ssa
trida
ctyla
6
0.51
−
4.10
*
1 Fr
eder
ikse
n et
al.
(200
4)
Whi
ncha
t Sa
xico
la ru
betra
55
2
Crick
and
Spa
rks
(199
9)
East
ern
blue
bird
Si
alia
sia
lis
25
−0.
15
* −
1.35
*
2 To
rti a
nd D
unn
(200
5), P
. Dun
n (u
npub
lishe
d da
ta)
Woo
d nu
that
ch
Sitta
eur
opae
a 29
.5
0.01
*
−0.
87
* 1
Wes
olow
ski a
nd C
hole
wa
(200
9)
Arct
ic te
rn
Ster
na p
arad
isaea
70
−
0.26
*
−3.
88
* 1
Møl
ler e
t al.
(200
6)
Colla
red
dove
St
rept
opel
ia d
ecao
cto
36
Crick
and
Spa
rks
(199
9)
Euro
pean
sta
rling
St
urnu
s vu
lgar
is 35
.3
−0.
01
−1.
82
* 2
Crick
and
Spa
rks
(199
9), R
ubol
ini e
t al.
(200
7)
Blac
kcap
Sy
lvia
atri
capi
lla
56
0.20
*
−5.
37
* 2
Crick
and
Spa
rks
(199
9)
Whi
teth
roat
Sy
lvia
com
mun
is 56
0.
13
* 2
Crick
and
Spa
rks
(199
9)
Tree
sw
allo
w
Tach
ycin
eta
bico
lor
40
−0.
28
* −
1.86
*
1 Du
nn a
nd W
inkl
er (1
999,
unp
ublis
hed
data
)
Win
ter w
ren
Trog
lody
tes
trogl
odyt
es
57
−0.
28
* −
3.88
*
2 Cr
ick a
nd S
park
s (1
999)
Blac
kbird
Tu
rdus
mer
ula
20
−0.
31
* 2
Nie
lsen
and
Møl
ler (
2006
)
Amer
ican
robi
n Tu
rdus
mig
rato
rius
50
0.14
−
2.21
*
2 To
rti a
nd D
unn
(200
5), P
. Dun
n (u
npub
lishe
d da
ta)
Song
thru
sh
Turd
us p
hilo
mel
os
34
−1.
23
* 2
Crick
and
Spa
rks
(199
9)
Mist
le th
rush
Tu
rdus
visc
ivor
us
57
−5.
21
* 2
Crick
and
Spa
rks
(199
9)
Com
mon
gui
llem
ot
Uria
aal
ge
20.5
0.
03
* 1
Fred
erik
sen
et a
l. (2
004)
, Ree
d et
al.
(200
9)
Thick
-bill
ed m
urre
Ur
ia lo
mvi
a 20
−
0.27
*
* 1
Gas
ton
et a
l. (2
009)
Mas
ked
lapw
ing
Vane
llus
mile
s 46
0.
00
−0.
01
1 Ch
ambe
rs e
t al.
(200
8)
Nor
ther
n la
pwin
g Va
nellu
s va
nellu
s 10
3 −
0.03
*
* 1
Crick
and
Spa
rks
(199
9), B
oth
et a
l. (2
005)
Aste
risks
indi
cate
sig
nifi c
ant
chan
ge in
layin
g da
tes
over
tim
e or
with
tem
pera
ture
. N y
ears
is t
he n
umbe
r of
yea
rs a
nalys
ed in
eac
h st
udy
(mea
ns f
or m
ultip
le s
tudi
es).
Layd
ate
chan
ge/y
ear
and
°C a
re t
he
slope
s of
regr
essio
n lin
es. N
bro
ods
is co
ded
as 1
= ty
pica
lly o
ne b
rood
, 2 =
typi
cally
two
or m
ore
broo
ds. B
lank
s in
dica
te n
o da
ta a
vaila
ble.