Supplementary Material
Host species identification and classification
A species was classified as a host if at least one documented case of cuckoo parasitism was reported
and it was classified as a suitable host in Table 1 of Moksnes and Røskaft (1995), where an
extensive review of the occurrence of cuckoo eggs in nests of European birds is presented. In
Moksnes and Røskaft (1995), suitable host species were considered as those that "have experienced
a co-evolutionary arms race with the cuckoo", as opposed to unsuitable hosts which were defined as
those breeding in cavities, feeding their young with food unsuitable for the cuckoo chick or with
eggs/nests too large to allow ejection of host eggs by the cuckoo. The rationale for considering a
species as a host even when only one or few cases of parasitism were documented, in the absence of
information on the number of nests sampled for hosts with low parasitism rates, is that such few
cases are unlikely to represent accidental 'mistakes' by the cuckoos if the species is "suitable" to
parasitism. No phenological information was available for any suitable host with no documented
parasitism by the cuckoo, and, therefore, these species were not considered. Main hosts (i.e. hosts
that account for most of the cases of cuckoo parasitism in different habitats and geographical
regions) are host species classified as such in Davies (2000) (all species listed on pages 27-28). No
detailed analysis in relation to parasitism rates could be performed due to extensive geographical
variation in host choice by the cuckoo (Davies 2000), although parasitism rates are significantly
repeatable among populations (Soler et al. 1999).
For each host species we recorded the migratory strategy, i.e. whether a species was a shortor long-distance migrant. Because of inter-population differences in migratory strategy (e.g. the
blackcap Sylvia atricapilla, Cramp 1998), this coding was not straightforward for some species.
Therefore, we defined a species as a long-distance migrant if most populations migrate to Africa or
the Middle East to winter, while all other species, mainly wintering within Europe or within the
Mediterranean basin, were categorized as short-distance migrants. Migratory strategy was classified
based on Cramp (1998).
The entire dataset including the list of host species, host classification, migratory strategy
and population trend (BirdLife International 2004; see also Møller et al. 2008) is reported in Table
S1.
Estimates of change in first arrival dates
We used phenological data on first arrival date (FAD) of the cuckoo and host species derived from
several sources (Table S2) during the period 1947-2007. The criteria for inclusion were that 1) the
study reported phenological information for the cuckoo and at least one host species; 2) the time
series contained data for at least 15 years; and 3) phenological data were collected at European sites
west of 30° E.
As in the great majority of cases we did not have access to original yearly phenological data,
but only to the FAD slope on year, the latter is therefore used as the dependent variable in the
analyses. Rate of change in FAD (in days/year) was expressed as the slope of the linear regression
of the yearly phenological data over the year of collection.
Most of the data derived from the database used by Rubolini et al. (2007) (see Table S2).
Additional slopes were taken from Croxton et al. (2006), Sparks et al. (2007) and Végvári et al.
(2009). In addition, we computed slopes of change in FAD from original data provided by L. V. S.
or from data reconstructed from graphs published in Gordo et al. (2005) and Schmidt and Hüppop
(2007). The accuracy of our method to reconstruct time series based on published graphs was
confirmed by cross-checking some of the reconstructed time series with the original data kindly
supplied by the authors (see Saino and Ambrosini 2008 for details).
Hosts for which only a single estimate of change in FAD was available were excluded. The
rates of change in FAD included in the present study were based on 340 time series with at least 16
years of data over at least 24 years from 20 sites. The host rate of change in FAD was available for
16 short-distance migrants (n = 93 estimates; mean number per species = 5.8 (3.19 s.d.)) and 26
long-distance migrants (n = 227; 8.7 (5.57 s.d.); see Table S1).The geographical distribution of time
series is shown in Fig. S1 and listed in Table S2.
Albeit data from different sites were collected adopting different degrees of standardization
and census methods (see details in original references listed in Table S2), we emphasize that within
each site the methods of data collection were consistent, and all sites included data for both the
cuckoo and some of its hosts. Anyway, our results were not confounded by such heterogeneity, as
suggested by within-site comparisons of the rate of change in FAD of the cuckoo and its short- or
long-distance migratory hosts, and by linear mixed model (LMM) analyses where site and species
were included as random effects (see below and Results).
Because phenological trends may have varied across years (see Rubolini et al. 2007),
inclusion of slopes derived from time series starting in different years between 1947 and 1984 (see
also Table S2) and of variable length may have introduced noise in the data. We controlled for these
potentially confounding effects by including year of start of the time series and number of years
with phenological data for each time series as covariates in LMM analyses of rates of change in
FAD (see below and Results).
It should also be emphasized that we used FAD, despite the potential pitfalls associated with
this metric of phenology (see Lehikoinen et al. 2004), because there was too limited information
concerning other metrics of timing of arrival (e.g. mean or median arrival dates). However, FAD
and mean arrival dates have been shown to be positively correlated in a recent review of the
available information for different species sampled at several sites throughout Europe (Sparks et al.
2005). In fact, the mean Fisher z-transformed correlation coefficients between FAD and mean
arrival dates was 0.513 (0.044 s.e.m.; n = 14), indicating that, in the absence of extensive data on
mean arrival dates, FAD can be used as a proxy for the general phenological trends of migratory
birds, as also assumed in a large number of previous studies (e.g. Mason 1995; Tryjanowski et al.
2002; Cotton 2003; Ahas and Aasa 2006; Croxton et al. 2006; Zalakevicius et al. 2006; Sparks et al.
2007; Hubalek and Capek 2008).
Importantly, estimates of FAD may be confounded by population trends and tend to be later in
declining species (see Miller-Rushing et al. 2008). To check for the robustness of our findings with
respect to this source of bias, we repeated the analyses while including only species that have
undergone a decline at least as large as that of the cuckoo (see below, “Analyses of FAD restricted
to declining hosts”).
Test for publication bias
A potential problem of meta-analyses is represented by publication bias (Rosenthal 1979), because
statistically significant results are more likely to be published than non-significant findings. This
should not be the case in our dataset because we have included for each source all the time series
satisfying selection criteria, irrespective of temporal trends in FAD (see also Rubolini et al. 2007).
In addition, as we only relied on multi-species studies, it seems unlikely that authors of published
studies have systematically excluded from their papers species which have shown no temporal trend
in FAD while including those that have exhibited significant changes in FAD. However, it is
possible that the published sources we have considered represented a non-random selection of
studies with respect to temporal trends in FAD, because studies reporting trends towards earlier
spring arrival of birds may be more likely to be published than those not reporting earlier spring
arrival. To test for this possibility, we adopted a dual approach. First, we tested whether the mean
within-site rate of change in FAD differed between the published (n = 15) or the unpublished (n =
5) sources (for SDM, LDM and the cuckoo separately) by means of independent samples t-tests (see
Table S2 for the list of sources). Secondly, we tested whether the average rate of advancement of
species differed between the published and unpublished sources, by means of paired t-tests. This
analysis was restricted to the 26 species (including the cuckoo) with at least two estimates of FAD
rate of change both for published and unpublished sources.
We found that the mean within-site rate of change in FAD did not differ significantly
between the published and unpublished sources, either for SDM (published: -0.381 (0.053 s.e.m),
unpublished: -0.398 (0.086), t12 = -0.17, p = 0.864), LDM (published: -0.127 (0.04), unpublished: 0.122 (0.033), t18 = 0.06, p = 0.954) or the cuckoo (published: -0.148 (0.052), unpublished: -0.085
(0.064), t18 = 0.64, p = 0.533). Similarly, the mean within-species rate of change in FAD did not
differ significantly between the published and the unpublished sources (paired t-test, t25 = 0.98, p =
0.34). These results strongly suggest that publication bias had little, if any, effect on our
conclusions.
Statistical analyses
The analyses were mainly based on mean pairwise differences in change in FAD between the
cuckoo and each host across study sites. However, these analyses could be biased if data on
advancement of arrival of short-distance migrants are relatively more abundant from areas where
advancement of migration dates has been larger, irrespective of migration strategy. Therefore, we
analyzed the rates of advancement by means of linear mixed models (LMM) with species and site
as random effects and a three-level fixed factor accounting for the species being a long-distance
migrant host, a short-distance migrant host or the cuckoo. In these models, year of start of the time
series and number of years with phenological data for each time series were included as covariates
(see above). The interactions between species category and these covariates were initially included
in the models and then excluded if non-significant. The above analyses were also run on the subset
of long-distance and short-distance migratory hosts that, according to BirdLife International (2004),
experienced a decline in population at least as large as that experienced by the cuckoo (see also
above). LMM analyses were run using SAS 9.0 statistical package. Moreover, we also conducted
the analyses by computing the mean rate of change in FAD of long-distance or short -distance
migratory hosts within each site and comparing these means to the rate of change in FAD of the
cuckoo for the same sites.
Analyses of FAD restricted to declining hosts
The analyses presented in the Results on the differences in the rate of change in FAD of the cuckoo
and its hosts were repeated on hosts that have experienced a population decline at least as large as
the cuckoo, according to BirdLife International (2004). The results are summarized below.
Test on the difference in FAD rate of change between cuckoo and suitable hosts (one-sample ttests):
SDM: t5 = 6.59, p = 0.001
LDM: t9 = -0.74, p = 0.477
Test on the difference in FAD rate of change between cuckoo and main hosts (one-sample t-tests):
SDM: t3 = 5.11, p = 0.014
LDM: t7 = -0.74, p = 0.484
LMM with species and site as random factors on suitable hosts accounting for the effects of year of
start and number of years of time series (covariates):
Effect of species category (cuckoo, SDM or LDM):
F2, 6.35 = 15.29, p = 0.004
post-hoc tests: cuckoo vs. SDM: p = 0.010; cuckoo vs. LDM: p = 0.959; SDM vs. LDM: p < 0.001
LMM with species and site as random factors on main hosts accounting for the effects of year of
start and number of years of time series (covariates):
Effect of species category (cuckoo, SDM or LDM):
F2,6.47 = 11.09, p = 0.008
post-hoc tests: cuckoo vs. SDM: p = 0.010; cuckoo vs. LDM: p = 0.911; SDM vs. LDM: p < 0.001
Correlation between migration and breeding dates
We extracted information on the week of start of main spring migration and egg laying periods
available in annual cycle diagrams in Cramp (1998) for the cuckoo host species included in this
study (see Table S1). These data were available for 30 of the 40 host species we considered. The
Spearman rank correlation between start of migration and start of breeding was 0.552, p = 0.002, n
= 30.
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Figure S1. Geographic location of sites for which we obtained information on change in cuckoo and
host arrival dates. Dot size is proportional to the number of cuckoo and host time series for each
study site.
Table S1. Information on migratory strategy (0 = short-distance migrant, 1 = long-distance
migrant), degree of cuckoo parasitism (1 = main host according to Davies 2000), and mean pairwise
differences of change in arrival dates between the cuckoo and its hosts across all sites. Population
trends reported by BirdLife International (2004) were coded as: moderate decline: -2; small decline:
-1; stable: 0; small increase: +1 (see also Møller et al. 2008). Species are sorted according to
migratory strategy, host category and alphabetical order of scientific name.
Species
Alauda arvensis
Anthus petrosus
Calcarius lapponicus
Lullula arborea
Anthus pratensis
Carduelis cannabina
Emberiza citrinella
Emberiza schoeniclus
Erithacus rubecula
Fringilla coelebs
Fringilla montifringilla
Motacilla alba
Phylloscopus collybita
Prunella modularis
Sylvia atricapilla
Troglodytes troglodytes
Anthus cervinus
Emberiza hortulana
Emberiza rustica
Hippolais icterina
Locustella fluviatilis
Locustella luscinioides
Locustella naevia
Luscinia luscinia
Luscinia megarhynchos
Luscinia svecica
Acrocephalus arundinaceus
Acrocephalus palustris
Acrocephalus schoenobaenus
Acrocephalus scirpaceus
Anthus trivialis
Lanius collurio
Motacilla flava
Muscicapa striata
Phoenicurus phoenicurus
Phylloscopus sibilatrix
Phylloscopus trochilus
Saxicola rubetra
Sylvia borin
Sylvia communis
Sylvia curruca
Sylvia nisoria
Main
host
0
0
0
0
1
1
1
1
1
1
1
1
1
1
1
1
0
0
0
0
0
0
0
0
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
Migratory
strategy
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
1
Difference
in FAD
0.321
0.158
0.294
-0.021
0.248
0.112
0.332
0.296
0.157
0.286
0.207
0.066
0.220
0.062
0.272
0.270
-0.307
0.074
0.356
-0.094
-0.158
0.006
0.085
-0.007
-0.063
0.014
-0.149
0.052
0.098
0.212
0.132
-0.097
-0.047
-0.048
-0.021
0.092
-0.009
-0.072
-0.026
-0.038
0.033
-0.092
n time
series
7
2
3
3
7
6
2
6
7
7
3
6
13
5
12
4
2
3
2
5
3
3
9
5
8
4
4
2
12
11
12
5
14
16
15
13
19
14
15
13
16
2
Population
trend
-1
-1
0
-1
-2
-1
-1
1
0
0
0
0
0
1
1
-1
-1
0
0
0
0
0
-1
0
0
0
-1
-1
-1
-1
0
-2
-1
-1
0
1
0
-
Table S2. Summary of sample sizes, geographical origin (coordinates in decimal degrees), and source of data included in the analyses. The change
in FAD of the cuckoo for each site is also shown (slope of the linear regression of FAD on year; positive values: delayed FAD; negative values:
earlier FAD), as well as the maximum time frame of the time series included in each study. Sites are sorted by decreasing latitude.
Site (country)
n suitable host
n main host
changes in FAD changes in FAD
Kemi (FI)
Turku (FI)
Jurmo (FI)
Rybachy (RU)
Vilnius (LT)
Zuvintas (LT)
Wharfedale (GB)
Parchim (DE)
Sheffield (GB)
Leicester and Rutland (GB)
Essex (GB)
Oxfordshire (GB)
Bristol (GB)
Sussex (GB)
Portland (GB)
Stutensee/Karlsruhe (DE)
Remstal (DE)
Bad Buchau (DE)
Hortobágy (HU)
Cardedeu (ES)
25
39
30
11
23
13
7
32
13
16
14
11
14
14
13
6
9
4
25
1
20
27
23
10
19
11
7
24
12
14
12
10
12
12
12
5
8
4
19
0
Total n slopes
Mean n slopes per site (s.d.)
320
16.0 (9.95)
261
13.1 (7.04)
Cuckoo change in
FAD (days/year)
Time
frame
0.008
-0.083
-0.021
0.002
-0.360
-0.333
-0.010
-0.243
-0.100
-0.020
0.010
-0.510
-0.010
-0.270
-0.004
-0.155
-0.343
-0.221
-0.278
0.300
1967-2001
1965-2000
1970-1999
1958-2005
1971-2004
1966-1995
1947-2002
1963-2006
1973-2002
1954-2002
1950-2002
1971-2000
1947-2002
1960-2002
1959-2005
1970-2003
1970-2003
1970-2003
1969-2007
1952-2003
Original reference
Coordinates
P. Suopajärvi et al. (unpub. data)a,b
E. Lehikoinen et al. (unpubl. data)a,c
E. Lehikoinen et al. (unpubl. data)a,d
L.V. Sokolov (unpubl. data)e,f
Zalakevicius et al. (2006)a
M. Zalakevicius (unpubl. data)a,g
Sparks et al. (2007)
Schmidt and Huppop (2007)
Sparks et al. (2007)
Sparks et al. (2007)
Sparks et al. (2007)
Cotton (2003)a
Sparks et al. (2007)
Sparks et al. (2007)
Croxton et al. (2006)
Peintinger and Schuster (2005)a
Peintinger and Schuster (2005)a
Peintinger and Schuster (2005)a
Végvári et al. (2009)
Gordo et al. (2005)
65.75 N, 24.53 E
60.43 N, 22.20 E
59.83 N, 21.62 E
55.17 N, 20.85 E
54.60 N, 25.30 E
54.43 N, 23.58 E
54.00 N, 2.00 W
53.70 N, 11.83 E
53.40 N, 1.40 W
52.60 N, 1.00 W
51.80 N, 0.60 E
51.75 N, 1.25 W
51.40 N, 2.60 W
51.00 N, 0.30 E
50.52 N, 2.45 W
49.08 N, 8.48 E
48.78 N, 9.73 E
48.08 N, 9.62 E
47.58 N, 21.15 E
41.57 N, 2.35 E
a: data included in Rubolini et al. (2007); b: details of data collection methods in Rauhala (1994); c: details of data collection methods in Lehikoinen et al. (2003); d: details of
data collection methods in Rainio et al. (2006) and Lehikoinen et al. (2003); e: details of data collection methods in Sokolov et al. (1998); f: included only time series with FAD
later than April 1st, with additional data for species included in Sparks et al. (2005); g: details of data collection methods in Zalakevicius and Zalakeviciute (2001).