Effects of climate change on timing of breeding and ... · Effects of climate change on timing of breeding and ... The mismatch hypothesis is ... date of peak caterpillar abundance

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113

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


114 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

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


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 115

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



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.



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



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



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



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



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.



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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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)


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.

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