Recent phenological shifts of migratory birds at a Mediterranean spring stopover site: Species wintering in the Sahel advance passage more than tropical winterers.

Spring migration phenology is shifting towards earlier dates as a response to climate change in many bird species. However, the patterns of change might not be the same for all species, populations, sex and age classes. In particular, patterns of change could differ between species with different ecology. We analyzed 18 years of standardized bird capture data at a spring stopover site on the island of Ponza, Italy, to determine species-specific rates of phenological change for 30 species following the crossing of the Mediterranean Sea. The advancement of spring passage was more pronounced in species wintering in Northern Africa (i.e. short-distance migrants) and in the Sahel zone. Only males from species wintering further South in the forests of central Africa advanced their passage, with no effect on the overall peak date of passage of the species. The migration window on Ponza broadened in many species, suggesting that early migrants within a species are advancing their migration more than late migrants. These data suggest that the cues available to the birds to adjust departure might be changing at different rates depending on wintering location and habitat, or that early migrants of different species might be responding differently to changing conditions along the route. However, more data on departure time from the wintering areas are required to understand the mechanisms underlying such phenological changes.

Introduction

Migration phenology in birds and other animals has been shifting in recent years, along with overall climate change [1-4]. This is a global phenomenon observed in all continents where enough long-term data are available [5-9]. In the Palaearctic-African bird migration system, most studies documented an advance in spring migration and arrival at the breeding grounds [10, 11] though changes in autumn migration have been observed as well [12, 13]. Both short- and long-distance migrants are affected [14-16] and changes are usually related to changes in the North Atlantic Oscillation Index (NAOI) and temperatures along the route [14, 17–27]. The pattern of phenology shift is complex, and species, populations, sexes and age classes are affected differently [28-36]. Timing effects might be more pronounced in certain areas than in others [32, 33, 37, 38], and in some cases they might have opposite trajectories [39], possibly underlining weather effects along the route [40]. In some cases, the early phases of migration are affected more strongly than the late ones [23, 39, 41, 42]. It is still debated whether phenology shifts are driven by microevolutionary changes or by phenotypic plasticity [10, 11, 43, 44], though the latter mechanism has recently received increasing support [45].

Some of the methods used for detecting switches in phenology have been object of debate [46, 47]. Studies using first arrival dates might overestimate changes, and several authors advised to use median and percentile passage dates to better describe the phenomenon [16, 48, 49]. The latter approach provides tools to understand and monitor in more detail the process of phenology shifts in spring migration, which is likely linked to climate change. Conditions in the African wintering grounds are changing, e.g. the Sahel zone is becoming greener (as predicted by [50, 51], and described in [52]), while stopover areas in Northern Africa are becoming drier ([53-55], but see [56]). This might be due to the recent trend towards a positive NAOI in the last years (https://www.ncdc.noaa.gov/teleconnections/nao/, last accessed on July 2nd, 2020). These environmental data suggest that species wintering in the Sahel and actively using stopover sites in Northern Africa might be more affected than others in their timing of passage, which should be reflected in an earlier arrival in Southern Europe.

Here, we aimed at identifying recent changes in migration phenology of migrants that cross the Mediterranean Sea, with a particular focus on within-species comparison between early and late migrants and on differences between species with different wintering areas. To this aim, we analyzed a large dataset of captures of migratory birds (nearly 220 000 individuals, mostly passerines) on spring migration from a small Italian island, where large numbers of individuals of several species are stopping over after crossing the Mediterranean Sea [57]. We calculated peak passage date and the dates of start and end of the main migration period for every year of the study, totaling 18 years, in 30 species of bird migrants. We determined the trends of change in these parameters for every species and tested for general patterns within groups of species based on their wintering range.

Study site and methods

Study site and ringing operations

This study was conducted on Ponza, a small island in the Tyrrhenian Sea (9.87 km2) located about 50 km off Italy (40°55’ N, 12°58’ E), where spring bird migration has been monitored since 2002 (www.inanellamentoponza.it). Ponza attracts large numbers of African-European migratory landbirds during spring migration as it is located along one of the main Mediterranean migratory routes, with daily peaks of over 1500 individual birds ringed occurring several times during the study period. Birds were caught using mist-nets from March (or April in some years) to May (exact start and end dates are shown in S1 Table). Ringing was conducted under permit from the Regione Lazio (Determinazione Dirigenziale B0332/06; B0084/09; A12042/11; G00575/15; and G00668/18). No ethical permit is required for standard capture and ringing. Ringing was conducted daily except for days with heavy rain or strong winds (>15 knots). These conditions occurred on <1% of the total ringing days over the entire study period. The mist-nets were checked hourly from dawn until one hour after dusk. The average total length of mist nets deployed was 227 m. We kept the net brand (Lavorazione Reti Bonardi, Monte Isola BS, Italy, http://www.vbonardi.it/) and model (2.4 m height, 16 mm mesh size) constant throughout the entire study period. The birds were ringed, aged and sexed according to the available literature [58, 59]. We analyzed 18 years (2002–2019) of capture data standardized by daily effort (Catch Per Unit of Effort, hereafter CPUE). For this analysis, we used data of the 30 most abundant species in number of individuals during the study period (Table 1). We divided the species in three groups based on their main wintering area, referring to [60, 61] for a description of their wintering areas. We divided them into species wintering mainly in North Africa (North of the Sahara Desert), the Sahel zone (dry scrubland just South of the Sahara Desert), and tropical Africa (Guinea savanna and tropical forests).

Table 1

Summary of the study species captured on the island of Ponza between 2002 and 2019 and used in the analysis.

Species	Total individuals captured	Average individuals per year [min, max]	Median passage (Julian day)	Wintering area
Acrocephalus arundinaceus	410	23 [4, 58]	124.2	Tropical
Acrocephalus schoenobaenus	1162	65 [17, 236]	127.1	Sahel
Anthus trivialis	2193	122 [19, 202]	108.4	Tropical
Erithacus rubecula	13044	725 [1, 2599]	86.5	North Africa
Ficedula albicollis	1548	86 [1, 279]	112.7	Tropical
Ficedula hypoleuca	10312	573 [65, 914]	115.8	Tropical
Hippolais icterina	6608	367 [45, 583]	109.4	Tropical
Hirundo rustica	507	28 [1, 67]	105.3	Tropical
Jynx torquilla	676	38 [17, 72]	121.0	Sahel
Lanius senator	1811	101 [11, 214]	105.3	Sahel
Luscinia megarhynchos	736	41 [13, 114]	120.7	Tropical
Merops apiaster	8654	481 [46, 1052]	130.4	Tropical
Muscicapa striata	18871	1048 [216, 2922]	134.3	Sahel
Oenanthe hispanica	127	7 [0, 25]	105.7	Sahel
Oenanthe oenanthe	2097	117 [21, 212]	105.7	Sahel
Oriolus oriolus	1404	78 [19, 182]	123.4	Tropical
Phoenicurus ochruros	1972	110 [0, 397]	83.1	North Africa
Phoenicurus phoenicurus	5474	304 [45, 726]	110.4	Sahel
Phylloscopus collybita	3809	212 [1, 589]	86.9	North Africa
Phylloscopus sibilatrix	14784	821 [159, 1430]	116.4	Tropical
Phylloscopus trochilus	12673	704 [83, 1321]	110.0	Sahel
Saxicola rubetra	16980	943 [455, 1647]	119.5	Tropical
Saxicola torquatus	564	31 [0, 147]	74.9	North Africa
Streptopelia turtur	564	31 [16, 49]	123.0	Sahel
Sylvia atricapilla	2303	128 [4, 574]	98.4	North Africa
Sylvia borin	49713	2762 [581, 5967]	130.2	Tropical
Sylvia cantillans	8019	446 [29, 1089]	97.2	Sahel
Sylvia communis	30496	1694 [500, 3594]	121.3	Sahel
Turdus philomelos	1828	102 [0, 477]	82.8	North Africa
Upupa epops	458	25 [1, 64]	91.9	Sahel

Total number of birds captured, yearly average with minima and maxima in brackets, median passage date expressed as Julian date (1 = January 1st), and main wintering area are indicated.

Analysis of passage timing

To define the peak date of passage and the time window encompassing the main migration period (hereafter referred as migration window), we used a 7-days Moving Average (MA) of the daily CPUE values for each species (see S1 Fig for a visual representation of the general patterns). For every year of the study and for each species separately, peak date of passage was defined as the day with the highest MA of migrating birds. The start and end of the main migration period were defined from the tail ends of the timing distribution as the dates when MA was below 10% of the peak value. In years when the ringing season started after the onset of the migration period (i.e. with smoothed data for the first day above 10% of peak MA) and/or ended before the end of the migration period (i.e. with smoothed data for the last day above 10% of peak MA) for any species, the tails of the distributions, and therefore the start or the end of the migration period, were not defined for that year and species. The width of the migration window was defined as the difference in days between the start and the end of the main migration period. Statistical analysis for changes in timing were made based on the annual values of start, peak and end of the main migration period, when available. Species-years where the total number of captures was lower than 5 were excluded from the analysis. This method is insensitive to the shape of the probability distribution of daily migration values and is therefore preferred over methods that rely on a pre-defined probability distribution (e.g. a normal distribution), and allows to identify migration peaks without relying on quantile measurements such as the median, which is not reliable in case of a truncated sample. S1 Fig shows that there is a nearby perfect overlap between the observed data and the fitted data using the MA method.

We analyzed changes in timing of the annual values of start, peak and end of the main migration period separately for every species using linear regressions. The slope of this regression indicates the average yearly change in date of passage on Ponza. Negative slopes indicate an advance in passage, while positive slopes indicate a delay. We compared the changes in passage dates of the three wintering groups (North Africa, Sahel, and Tropical Africa) using linear mixed effects models (LMM) with respectively start, peak, end of migration period, and migration window as response variables, and wintering group, year, and the interaction between wintering group and year as fixed effects, while species was used as a random effect. A significant interaction indicates different slopes of passage date over the years in the different groups. To test for pairwise differences, we first estimated the marginal means of the linear trends between wintering group and year using the emtrends function of package emmeans in R [62]. We then used the cld function of package multcomp [63] to compare these means pairwise among groups. This function groups the different levels of a variable (in our case the wintering groups) according to a set p-level, which is 0.05 by default. To estimate the p-level of non-significant pairwise comparisons we therefore had to change the p-level for grouping, thus resulting in p-values that are within a range rather than being exact (see Results). For the comparison of the start of the migration period and the migration window, we excluded the species wintering in North Africa, since for most of them the date of start of passage was not estimated.

Sex could be determined based on morphology in 11 species (1 from North Africa, 4 from the Sahel, and 6 from Tropical Africa). In these species, in addition to the analysis described above, we performed separate linear regressions for each sex in every species. We then compared species wintering in the Sahel and in Tropical Africa (we excluded the only species from North Africa for this analysis) in the slopes of the peak date of passage separately for males and females, using LMMs with peak date of passage as a response variable, year, wintering group, and the interaction term of year and wintering group as fixed effects, and species as random effect. Again, a significant interaction term would imply a different slope in the change over the years, and we compared groups using the same procedure as described above. We also compared males and females within each wintering group in a similar fashion, this time using sex, year, and the interaction of sex and year as fixed effects. All analyses were performed using R 4.0.0 (www.r-project.org).

Results

The slopes of change in passage dates for each species are shown in Table 2 and visualized in S2 Fig. During the study period, peak date of passage was advanced significantly in 5 of the 30 species used in our analysis (3 from the North African wintering group, 2 from the Sahel group), with additional two species with an advance that was close to significance (both from the Sahel group). The range of yearly advance in peak date of passage (for significant trends only) was between 1.0 and 1.4 days per year.

Table 2

Summary of the changes (in days per year) of start, peak, end date of the main migration period and migration window for 30 bird species migrating through the island of Ponza between 2002 and 2019.

Species	Start [days/year]	Peak [days/year]	End [days/year]	Migration window [days/year]
Wintering group: North Africa
Erithacus rubecula	NA	-1.0 ± 0.4*	-0.5 ± 0.4	NA
Phoenicurus ochruros	NA	-0.4 ± 0.3	-0.3 ± 0.4	NA
Phylloscopus collybita	NA	-1.3 ± 0.5*	-0.3 ± 0.6	NA
Saxicola torquatus	NA	-0.4 ± 0.3	0.2 ± 0.3	NA
Sylvia atricapilla	NA	-0.3 ± 0.4	-0.3 ± 0.4	NA
Turdus philomelos	NA	-1.3 ± 0.6*	-0.1 ± 0.8	NA
Wintering group: Sahel
Acrocephalus schoenobaenus	-0.2 ± 0.4	0.3 ± 0.3	0.0 ± 0.9	-0.5 ± 1.3
Jynx torquilla	-1.5 ± 0.5*	-0.3 ± 0.5	-0.4 ± 0.3	1.2 ± 1.0
Lanius senator	0.1 ± 0.3	-0.2 ± 0.3	0.6 ± 0.4	0.5 ± 0.3
Muscicapa striata	-0.2 ± 0.4	0.5 ± 0.3	NA	NA
Oenanthe hispanica	-0.3 ± 0.4	-1.2 ± 0.7	-1.6 ± 0.5*	-1.2 ± 0.7
Oenanthe oenanthe	-0.1 ± 0.5	-0.7 ± 0.6	-0.2 ± 0.3	-0.1 ± 0.6
Phoenicurus phoenicurus	-1.6 ± 0.5*	-1.4 ± 0.5**	-0.1 ± 0.3	0.2 ± 0.8
Phylloscopus trochilus	0.0 ± 0.8	-0.7 ± 0.4	0.3 ± 0.2	0.0 ± 1.0
Streptopelia turtur	-0.3 ± 0.3	-0.1 ± 0.3	0.2 ± 0.4	0.5 ± 0.8
Sylvia cantillans	0.6 ± 1.0	-1.0 ± 0.4*	-0.1 ± 0.5	-2.4 ± 0.8
Sylvia communis	-0.5 ± 0.3	-0.1 ± 0.3	-0.2 ± 0.7	0.7 ± 1.0
Upupa epops	-1.3 ± 0.5*	-1.1 ± 0.5	0.7 ± 0.6	3.9 ± 1.1*
Wintering group: Tropical Africa
Acrocephalus arundinaceus	-0.7 ± 0.2**	-0.6 ± 0.4	0.1 ± 0.2	0.7 ± 0.4
Anthus trivialis	-0.7 ± 0.6	-0.5 ± 0.3	-0.2 ± 0.3	0.8 ± 1.4
Ficedula albicollis	-0.8 ± 0.5	-0.4 ± 0.4	-0.2 ± 0.3	0.5 ± 0.7
Ficedula hypoleuca	-0.7 ± 0.3*	0.1 ± 0.3	0.5 ± 0.2*	0.8 ± 0.4
Hippolais icterina	0.2 ± 0.2	0.4 ± 0.3	0.3 ± 0.7	0.2 ± 1.4
Hirundo rustica	-1.7 ± 0.4**	-0.5 ± 0.5	0.0 ± 0.3	2.6 ± 0.8*
Luscinia megarhynchos	-0.5 ± 0.4	-0.4 ± 0.4	0.1 ± 0.3	0.7 ± 0.8
Merops apiaster	-0.3 ± 0.2	-0.1 ± 0.3	0.1 ± 0.3	0.4 ± 0.4
Oriolus oriolus	-0.2 ± 0.2	0.4 ± 0.3	NA	NA
Phylloscopus sibilatrix	-0.3 ± 0.4	0.3 ± 0.3	0.3 ± 0.2	1.2 ± 0.7
Saxicola rubetra	-0.6 ± 0.3	0.1 ± 0.3	0.1 ± 0.1	0.6 ± 0.5
Sylvia borin	-0.3 ± 0.3	0.2 ± 0.3	NA	NA

Slopes ± SE from the linear regression of date by year are given. Significant slopes are represented in bold typeface.

** = p < 0.01

* = 0.01 < p < 0.05. Exact p-values are shown in S2 Table. Negative values indicate an advanced passage. In the last column (Migration window), the magnitude of the change in width of the migration window is shown. Positive values indicate a broader migration window. NA indicates missing values when either start or end of the main migration period were not assessed.

The start of the main migration period was significantly advanced in 6 species (3 from the Sahel group, 3 from the Tropical group), and close to significance in one additional species (from the Tropical group). Note that the start of the migration period was not determined in any of the species in the North African group due to fact that their passage almost invariably began before the start of the capture season on Ponza. The range of yearly advance in the start of migration was between 0.7 and 1.7 days per year.

There was a significant advance of the end of the migration period by 1.6 days per year in one species from the Sahel group, and a significant delay in the end of migration by 0.5 days per year in one species from the Tropical group. One species from the Sahel group had a close to significant delay in the end of the migration period.

The migration window was significantly broadened in two species (one from the Sahel and one from the Tropical group), while the broadening of the migration window was close to significance in one additional species from the Tropical group. In one species from the Sahel group, the migration window was almost significantly narrower.

The marginal mean slopes of the peak date of passage change per year were significantly different from zero in two of the wintering groups (North Africa: -0.8 ± 0.2 days per year, p < 0.001; Sahel: -0.5 ± 0.1 days per year, p < 0.001), while this was not the case for the Tropical group (-0.1 ± 0.1 days per year, p = 0.433) (Fig 1). The slopes of the North Africa and the Tropical groups differed significantly from each other (cld comparison: p < 0.05), while the difference between the Sahel and the Tropical groups was marginally non-significant (0.05 < p < 0.06). The slope of the Sahel group and of the North Africa group did not differ from each other (0.20 < p < 0.25). The overall effect of year across species on the peak passage was significant in the LMM (t = -4.283).

Fig 1

Trends of change in start, peak, and end date of the main migration period of 30 bird species migrating through the island of Ponza between 2002 and 2019, subdivided into wintering groups.

Every dot represents the passage date of a single species in any given year. Patterns for all species singularly are shown in S1 Fig.

Peak date of passage was advanced overall in males (LMM: t = -3.081, Fig 2) but the slopes did not differ between Sahel and Tropical wintering birds (LMM; t = 1.149). The marginal mean slope of peak date of passage for males of the Sahel group was significantly different from zero (-0.7 ± 0.2 days per year, p = 0.002) and marginally non-significant in males of the Tropical group (-0.3 ± 0.2 days per year, p = 0.061). In females, there was both an overall effect of year on peak date of passage (LMM: t = -2.609, Fig 2) and on the interaction between year and wintering group (LMM; t = 2.382). The marginal mean slope of peak date of passage for females of the Sahel group was significantly different from zero (-0.6 ± 0.2 days per year, p = 0.010) and non-significant in females of the Tropical group (0.1 ± 0.2 days per year, p = 0.559).

Fig 2

Trends of change in the peak date of the main migration period on Ponza of males and females from 4 species wintering in the Sahel and 6 species wintering in tropical Africa.

Every dot represents the passage date of a single species in any given year.

When comparing sexes within the Sahel wintering group, there was no difference in slope between males and females (LMM: t = -0.253), while the slopes were different between sexes in the Tropical wintering group (LMM; t = -2.050). At the species level, peak date of passage was advanced significantly in both males and females of two species in the Sahel wintering group (Table 3).

Table 3

Summary of the changes (in days per year) in the peak date of the main migration period of 11 sexually dimorphic migratory bird species on Ponza between 2002 and 2019, divided by sex.

	Males		Females
Species	Peak ± SE	p	Peak ± SE	p
Wintering group: North Africa
Sylvia atricapilla	-0.3 ± 0.5	0.618	-0.6 ± 0.4	0.166
Wintering group: Sahel
Lanius senator	-0.1 ± 0.4	0.856	0.9 ± 0.5	0.082
Oenanthe oenanthe	0.0 ± 0.6	1.000	-0.5 ± 0.5	0.364
Phoenicurus phoenicurus	-1.6 ± 0.5	0.004**	-1.1 ± 0.5	0.046*
Sylvia cantillans	-1.0 ± 0.5	0.045*	-1.5 ± 0.4	0.004**
Wintering group: Tropical Africa
Ficedula albicollis	-0.9 ± 0.4	0.053	0.0 ± 0.4	0.918
Ficedula hypoleuca	-0.4 ± 0.2	0.136	0.2 ± 0.2	0.484
Hirundo rustica	-0.2 ± 0.6	0.779	-0.2 ± 0.6	0.710
Merops apiaster	-0.3 ± 0.4	0.396	0.1 ± 0.3	0.861
Oriolus oriolus	-0.2 ± 0.3	0.463	0.3 ± 0.4	0.382
Saxicola rubetra	-0.1 ± 0.2	0.575	0.3 ± 0.2	0.280

Negative values indicate an advanced passage. Significant slopes are represented in bold typeface.

** = p < 0.01

* = 0.01 < p < 0.05.

Both the Sahel and the Tropical wintering groups significantly advanced the start of the migration period (Fig 1), so that there was an overall significant effect of year (LMM: t = -3.766), but the slope was not different between the two groups (LMM: t = -0.214). The marginal mean slopes were -0.5 ± 0.1 days per year in the Sahel group (p < 0.001) and -0.5 ± 0.1 days per year in the Tropical group (p < 0.001).

The marginal mean slope of the change in the end of the migration period was not significantly different from zero in any of the wintering groups (North Africa: -0.3 ± 0.2 days per year, p = 0.074; Sahel: -0.1 ± 0.1 days per year, p = 0.678; Tropical: 0.1 ± 0.1 days per year, p = 0.373). There was no overall effect of year across species in the end of the migration period (LMM: t = -1.793) (Fig 1).

The migration window was broadened overall by 0.5 ± 0.3 days per year, though not significantly so (LMM: t = 1.818). There were no differences between wintering groups (LMM; t = -0.662) nor in the slopes of change between groups (LMM; t = 0.653).

Discussion

After having been reported in a large number of studies in the early 2000’s [10, 11], the advance of spring passage in migratory European-African migratory birds has received decreased attention, in particular in the Mediterranean basin. However, our results clearly show that this phenomenon is still ongoing, and it is occurring at a substantial rate. The values of yearly change in our study should be considered with caution for species with relatively low numbers of yearly captures or species for which data were not obtained every year. However, the robust overall results indicate that on average the peak of passage has been advanced by up to one day per year. The advance was most marked in species wintering in North Africa and, to a lesser extent, in those wintering in the Sahel zone. The peak of passage did not change markedly in species spending the winter in tropical Africa. While there was evidence for an advancement of the beginning of the migration period, the end did not change substantially. This results in a substantial though non-significant increase of the width of the migration window. For example, if we consider the Sahel group in our study, the average migration window changed from ~25 to ~40 days (Fig 1).

The pronounced advance in the peak date of passage in species wintering in North Africa confirms earlier findings that suggested that species not crossing the Sahara are able to better track changing conditions in the breeding grounds [64]. Given the phenological shift in plant productivity and the related change in peak prey abundance for insectivores [65], this result was not surprising. Improved conditions in the Sahel might be responsible for the advancement of migration dates also in species spending the winter in that area. Moreau [66] observed that migratory birds arrive to the Sahel zone at the beginning of the dry season, and throughout the winter they face deteriorating conditions that reach their negative peak when birds are preparing for spring migration. Recent winter rains may have relaxed this situation and allowed for richer foraging conditions during this critical time. Earlier departure with increasing winter rains in the Sahel has been shown for several species in past studies [67]. Interestingly, peak date of passage did not change over the period of the study in species wintering in the forested areas of tropical Africa. These are also the species that start their migration last since migration date is correlated with wintering latitude [68]. In general, the recently described re-greening of the Sahel zone [52, 69] might favour species that extensively use this region as a wintering area or as a stopover site during migration, by allowing faster refueling rates and thus earlier departure [70, 71]. Overall, environmental conditions in the wintering areas are the most likely factor determining regional differences in phenological adjustments. Future studies should address climatic changes in different regions within the wintering range of Eurasian-African migratory species to better understand these patterns.

The earlier start of the migration passage in Ponza is likely due to an earlier departure of the first migrants within each species [10]. The first birds to leave the wintering grounds are usually males [72, 73] and birds belonging to more temperate populations [74]. Our data suggest that both mechanisms play a role. In species wintering in the Sahel, both males and females advanced their peak date of passage, while in species wintering in tropical Africa, this only happened in males. While an increase in protandry seems to explain the earlier passage of tropical winterers, this does not seem to be the explanation for Sahel species. In the latter species, early departing individuals might have advanced their passage while late departing individuals, which possibly originated from more Northern populations [74], did not. There is evidence that individuals do not vary their migration timing over the years [34, 75–80], though this is not true for all species, especially in the case where individuals are able to track environmental cues to adjust their departure [81-84]. The role of phenotypic plasticity in individual departure as opposed to population-specific selection on early departing individuals needs to be further studied for each individual species.

Another explanation for the increased gap between first and last passage migrants is faster migration of the first migrants and/or slower migration of the last ones. There is high variability in the geographical patterns of migration within species and individuals [76, 80], and birds might undertake detours to track favourable habitats along the route [85]. van Noordwijk [86] suggested that faster migration could be achieved by skipping stopovers along the route. Deteriorating conditions in the Sahara Desert or in Northern Africa may cause less efficient stopover and thus an earlier departure, leading to an earlier arrival on Ponza. A skew of the passage phenology towards early migrants would also occur if conditions in Africa affected early migrants differently than late migrants. Northern Wheatears on the neighboring island of Ventotene show better body condition late in the season [74]. This indicates that late migrants might encounter more favourable conditions for refueling in Northern Africa than early migrants.

We do not know whether the change in passage dates on Ponza directly reflects a change in arrival on the breeding grounds. Most birds do not spend more than one day on Ponza before resuming migration [87], thus if they were to delay arrival to their territories, they would have to extend their stopover later on the continent. However, the strong carry-over effects of migration phenology on breeding events [88] indicate that differences in timing observed on Ponza should indeed reflect, at least to a certain extent, the differences in arrival to the breeding grounds. There is some evidence that the change in date of arrival at the breeding grounds in Europe is less steep than the change of passage in the Mediterranean [10, 32, 89], indicating that birds might slow down the pace of their migration when approaching the breeding grounds to fine-tune their arrival. Laying dates have advanced in relation to temperature changes at the breeding grounds [90, 91], to a smaller extent in long-distance compared to short-distance migratory species [92]. The passage data from Ponza confirm this observation, indicating that adjustments to the changing climate might be less pronounced in species wintering the furthest away from their breeding grounds.

Trans-Saharan migratory species show decreasing population trends in many of their breeding grounds in Europe [93, 94]. One of the causes of this decline is the phenological mismatch between the availability of prey at the breeding grounds and the arrival and consequent start of breeding of the birds [95]. The available data do not allow us to draw conclusions about the causes of the intraspecific differences and the mechanisms involved, but they are helpful for developing hypotheses and design future studies. The results of our study call for an intensification of data collection in the form of year-round tracking and long-term data sets at a large geographical scale. More data about the ecology of species, especially in the wintering quarters, are required to understand the selective pressure acting on migration timing, and to predict future changes and how these will affect population processes.

Frequency distribution of captures by date (Julian day: 1 January = day 1) for 30 species on the island of Ponza between 2002 and 2019.

Average CPUE per day are represented by the black lines, while the moving average is represented by the blue curve. This figure only illustrates general patterns. Note, however, that peak, start, and end of the main migration period were calculated for every year separately for the analysis of timing patterns.

(TIF)

Click here for additional data file.

Yearly dates of passage of 30 species on the island of Ponza between 2002 and 2019.

The blue lines represent the regression line of the start and end of the main migration period, while the black line represents the regression line for peak passage. Black dots represent yearly peak passage dates, while the whiskers represent start and end of the main migration period for every year of the study.

(TIF)

Click here for additional data file.

Start and end date of capture operations on Ponza during the 18 years of the study.

(DOCX)

Click here for additional data file.

p-values of the linear regressions of passage date and year for 30 species migrating through Ponza between 2002 and 2019.

Slopes and SE are shown in the main text in Table 2.

(DOCX)

Click here for additional data file.

25 May 2020

PONE-D-20-09340

Recent phenology shifts of migratory birds at a Mediterranean spring stopover site: birds wintering in the Sahel advance passage more than tropical winterers

PLOS ONE

Dear Dr. Maggini,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

The Reviewers made a great work and provided detailed and useful comments. Please consider all them because the suggested changes will add to the quality of the paper. In particular, I strongly advise you to consider with particular attention the comments regarding:

Reviewer #1

A formal comparison between different categories (long vs. short distance migrators, males vs. females)

Full reporting of all effects in statistical models, including the non-significant ones

Emphasizing the relevance of documenting an advancement in spring migration also in very recent years

Adding reference to recent literature (please note that the Reviewer very kindly provided a list of potentially relevant and recent papers)

Reviewer #2

Defend or discuss the statistical approach used to estimate phenology

Add details on the extent to which fieldwork could be performed according to the expected protocol

The major comment by Reviewer #2 deserves also consideration. Adding information on conditions at wintering sites or on passage areas across the Mediterranean would clearly add a lot of interest to the work.

Please submit your revised manuscript by Jul 09 2020 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.

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If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols

We look forward to receiving your revised manuscript.

Kind regards,

Roberto Ambrosini, Ph.D.

Academic Editor

PLOS ONE

Minor comments:

In Table 1 Oenante oenante is written with the species name capitalized. Please correct.

In line 126 and throughout the manuscript please replace “to anticipate” with “to advance”.

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Partly

Reviewer #2: Yes

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: No

Reviewer #2: N/A

**********

3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: No

Reviewer #2: No

**********

4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The study entitled “Recent phenology shifts of migratory birds at a Mediterranean spring stopover site: birds wintering in the Sahel advance passage more than tropical winterers” reports the description of the temporal variation in the dates of passage during the pre-nuptial migration of 18 bird species in a small island of the Mediterranean sea (Ponza). The main result is that most of the species under investigation advanced their passage time, and therefore add to the hundreds of studies reporting similar findings elsewhere in the globe. It also shows that species that migrate longer distances show a smaller temporal variation in phenology (e.g. the slope of the passage date against year) than those migrating further, as well as that males generally show steeper trends than females. The study is merely descriptive but worthy for a least two reasons: 1) it is conducted at an important passage site of which no information on migration time was available to date, and 2) because it was conducted in a rather recent period (2002-2019), and it therefore shows that birds are still shifting their phenology (and I think that this important result is not emphasized enough in the current version of the paper; please see below). I am therefore generally positive about the possibility that the paper would be accepted for publication. However, I am some issues that I would like to raise below in order to improve, I hope, the quality and the readability of the manuscript. I think that they should be easily addressed by the authors.

1) Statistical analyses and implications of the results. The conclusions are reasonable and compatible with the wide literature about the topic. However, I am not sure that the authors could claim that their study shows difference in the phenological variation between the species wintering in Northern Africa and in the Sahel zone and those wintering further South in the forests of central Africa without properly testing for it. I therefore encourage them adopt a proper statistical test in order to check for differences among groups of birds showing different migration strategies (and/or different wintering regions). This is also the case for the supposed differences between the phenology of males and females of some species. I am aware that the number of the species included in the analyses in not very large, but I think that there is the scope for splitting the species at least into two categories. However, if the authors think that this is not possible, in my opinion they should at least justify why they cannot analyse the data and add a caveat in the Discussion by acknowledging the reader about the limitations of their results.

2) Main migration period. The study is focused on the start, end, duration and peak of the so-called ‘main migration period’. The procedure used to define this period seems accurate to me, and it is not my intention to question it. However, since the vast majority of the hundreds of studies on migration phenology published to date usually focus on mean/median and/or first (as well as last) passage dates, I am wondering why the authors opted for this different procedure, which make their results difficult to be compared with the previous ones. I would suggest to at least better justify this decision and to provide some solid reasons why this procedure is better, at least for the case under study, than that used in most of literature.

3) Tables. I have also a concern about how tables have been completed. Frankly, I do not agree with reporting only significant relationships in the tables. I think it is important to report all the associations, including non-significant ones. This good practice is important, for example, to limit publication bias in meta-analytic studies. I therefore strongly encourage the authors to fully fill the tables. In addition, since the main message of the paper is a link between migration strategy and phenological change, I also think that it would be very helpful for the readers (especially for those non-expert in birds) to have some additional information about the species in the first part of the manuscript (other than in the Discussion where they are now reported). A possibility is to add a column in Table 1 reporting the migratory behaviour and/or the main wintering region of each species.

4) Introduction. On the whole, it is concise and well written. However, I was rather surprised not to read any clear mention about the effect of migratory behaviour on variation in migration phenology, also considering that the authors explicitly referred to short- and long-distance migrants in the Discussion. I understand that the authors mentioned where different species spend the wintering period, but information might not be enough for a generalist reader. According to literature, change in phenology depending on migratory behaviour is one of the most consolidated knowledge on the effect of climate change on birds. I would therefore encourage the authors to add a short paragraph on this (including relevant references), linked to that one focused on the effects of NAOI and wintering areas.

5) Discussion. As briefly mentioned above, I think that one the main interesting point of the study is that migration data have been collected rather recently. I think that the paper would benefit from the inclusion of an additional paragraph where the authors emphasize that the phenological shifting is still ongoing and compare their recent trends with those obtained by previous studies performed on very long time-series (e.g. Askeyev et al. 2009. Climate Research, 38: 189-192; Kolářová et al. 2015. Climate Research, 63: 91-98).

6) Literature cited. References quoted in the paper are generally relevant. However, I noted that only a few very recent papers (after 2015) have been cited, despite the vast literature produced in the last years. This is especially the case for Introduction, in which some very relevant and recent papers are missing. I therefore suggest to add some of them in order to better introduce the concepts, which will be developed through the manuscript. Please, find below some missing articles which are very relevant to the purpose of the study, and deserve to be cited (in chronological order).

- Kluen, E., Nousiainen, R., & Lehikoinen, A. (2017). Breeding phenological response to spring weather conditions in common Finnish birds: resident species respond stronger than migratory species. Journal of Avian Biology, 48(5), 611-619.

- Samplonius, J. M., Bartošová, L., Burgess, M. D., Bushuev, A. V., Eeva, T., Ivankina, E. V., ... & Mänd, R. (2018). Phenological sensitivity to climate change is higher in resident than in migrant bird populations among European cavity breeders. Global change biology, 24(8), 3780-3790.

- Ambrosini, R., Romano, A., & Saino, N. (2019). Changes in migration, carry-over effects, and migratory connectivity. Effects of Climate Change on Birds, 93.

- Radchuk, V., Reed, T., Teplitsky, C., Van De Pol, M., Charmantier, A., Hassall, C., ... & Avilés, J. M. (2019). Adaptive responses of animals to climate change are most likely insufficient. Nature communications, 10(1), 1-14.

- Horton, K. G., La Sorte, F. A., Sheldon, D., Lin, T. Y., Winner, K., Bernstein, G., ... & Farnsworth, A. (2020). Phenology of nocturnal avian migration has shifted at the continental scale. Nature Climate Change, 10(1), 63-68.

Minor comments:

LL 62-65. Maybe add some references here.

L 74. “near-passerine”. I think this should be defined, especially in a very generalist journal like the present one.

LL 89-92 and Table 1. It is ok to include information about the total number of individuals captured per species. However, because the authors declared that they selected the species to be included in the analyses based on the yearly number of captures, I think that an important missing information is also the range of individuals captured per species per year. In addition, it is not clearly described which criterion was used to decide whether including or not a species. For example, what is the minimum number of specimens per year? In addition, did the authors exclude some years within species because they could not collect information on a minimum number of individuals? In my opinion, all this information should be added to improve the understanding of the procedures used.

LL 113-115. Interesting that all the species show a significant temporal variation (advance or delay) in the phenology of migration. This is a quite unexpected result, if we compare it with the available literature. How do the authors explain this result? Is possible that the procedure used to identify the main migration period has somehow affected this result?

L 244. Publication number XX. Maybe there is an error here.

Reviewer #2: This paper aims to analyse the spring migratory phenology of 30 species of birds in a Mediterranean island, for a period of 18 years. Authors found a broadening of the time of passage overall, due to an advancement of the passage by mostly short-distance migrants.

The paper is well written, it is easy to follow and the concepts and literature used are within the expected current state of the art. A have, however, some comments to do:

Main comments:

The data set used in the study is impressive, and this is a robustness of the paper. However, the paper is totally descriptive, and the authors ‘only’ analyse a linear effect of year on the object, dependent variables (annual values of the start, peak and end of migration period). It would be really nice (though I acknowledge that this would entail much more work) if the authors may also look for the potential effects of conditions at wintering sites or during the passage across the Mediterranean. These analyses would allow a richer discussion around the observed changes/results. This is what I would also expect in a journal like PLOS ONE.

Minor comments:

L94-96. Quite often, mist nets must be closed due to very adverse weather (heavy rain, too strong winds) or even logistical reasons (lack of personal in given moments). Even though the authors say that the fieldwork was done on a daily basis, I would like to know to what extent this protocol was done with a 100% of, most likely, whether there were some gaps. In these cases, many authors think that replacing raw data by theoretical distribution regressions is better, since these last allow to: deal with gaps in the data set and smooth the potential effects of the variables affecting capture rates (e.g., birds are more likely to be capture in days without wind, or in cloudy mornings as compared to very sunny days). Furthermore, these theoretical distributions would also allow dealing with years when the campaign started after the onset of migration, or ended before its end. Authors should discuss/defend their statistical approach and explain why not dealing with the use of theoretical distribution curves.

L103. A good reason to use theoretical curves?

L106-109. For me, this would be an insufficient explanation. There can be other distribution curves that might fit reasonably well to your data.

L139. Please, this should be mention in Methods section.

L157. Overall, the discussion might be benefited if the authors would also consider to test for the effects of conditions in the wintering/passing areas on their dependent variables.

Table 1. Please, add SE to the beta parameter estimtes (slope).

Table 2. Too many NAs in the start and end of migration. Why? Maybe this might be improved by using theoretical curves? If not, please limit the analyses to the peak passage parameter.

**********

6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

8 Jul 2020

Please find our answers to the reviewers' and editor's comments in the attached file.

Submitted filename: Response to reviewers_final_final.docx

Click here for additional data file.

11 Aug 2020

PONE-D-20-09340R1

Recent phenological shifts of migratory birds at a Mediterranean spring stopover site: species wintering in the Sahel advance passage more than tropical winterers

PLOS ONE

Dear Dr. Maggini,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

This new version was revised by the Reviewer that raised the most serius concerns on the first version. He/she was rather satisfied by this new version, but he/she also asked for some further minor changes. We think you can easily modify the manuscript to acccount for these further suggestions. Please submit your revised manuscript by Sep 25 2020 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.

A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.

An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols

We look forward to receiving your revised manuscript.

Kind regards,

Roberto Ambrosini, Ph.D.

Academic Editor

PLOS ONE

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: I am rather satisfied by the revision made by the authors because they provided all the main suggested changes to the manuscript. In my opinion, the paper has considerably improved and I therefore suggest it for publication. I have only a few additional minor comments (lines numbers refer to the version including track changes):

LL 151-152. Please add references used to define wintering areas and to associate species to them.

L 211.5 rather than 22…a huge difference!

LL 211-237. The reader is lost until the last line of this long paragraph because the table and the figure are cited only at end. I suggest to mention them before.

L 237. Fig. S2, not S2 Fig.

Table 2. I am not sure that P values between 0.05 and 0.10 should be mentioned in a table, even considering that exact P-values are provided in the supplementary materials.

LL 383-384. There is some evidence that in many species the advance in arrival date in the breeding area is less steeper than the passage date in the Mediterranean area. This point might deserve a short discussion and some references (please see below).

Both, C. (2010). Flexibility of timing of avian migration to climate change masked by environmental constraints en route. Current Biology, 20(3), 243-248.

Jonzén, N., Lind´en, A., Ergon, T., Knudsen, E., Vik, J.O., Rubolini, D., Piacentini, D., Brinch, C., Spina, F., Karlsson, L., Stervander, M., Andersson, A., Waldenstr¨om, J., Lehikoinen, A., Edvardsen, E., Solvang, R. & Stenseth, N. C. (2006). Rapid advance of spring arrival dates in long-distance migratory birds. Science 312, 1959–1961.

Bitterlin, L. R., & Van Buskirk, J. (2014). Ecological and life history correlates of changes in avian migration timing in response to climate change. Climate Research, 61(2), 109-121.

LL 390-391. A very important study to be cited here is: Dunn, P. O., & Møller, A. P. (2014). Changes in breeding phenology and population size of birds. Journal of Animal Ecology, 729-739.

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

12 Aug 2020

Reviewer #1: I am rather satisfied by the revision made by the authors because they provided all the main suggested changes to the manuscript. In my opinion, the paper has considerably improved and I therefore suggest it for publication.

We thank the reviewer for the renewed assessment of our manuscript, and especially for her/his comments on the previous version that helped us to largely improve this new version.

I have only a few additional minor comments (lines numbers refer to the version including track changes):

LL 151-152. Please add references used to define wintering areas and to associate species to them.

The references are given in line 95 (new line numbering)

L 211.5 rather than 22…a huge difference!

We agree. This was due to a mistake in the previous analysis that we corrected in the new version. In the previous version, the large number of significant slopes caught the attention of the reviewers and was highly unlikely.

LL 211-237. The reader is lost until the last line of this long paragraph because the table and the figure are cited only at end. I suggest to mention them before.

We moved the reference to table and figure at the beginning of the paragraph.

L 237. Fig. S2, not S2 Fig.

This was suggested in the information for authors. We will change this if requested.

Table 2. I am not sure that P values between 0.05 and 0.10 should be mentioned in a table, even considering that exact P-values are provided in the supplementary materials.

We removed the highlights from slopes with p between 0.05 and 0.10 (we did the same in Table 3).

LL 383-384. There is some evidence that in many species the advance in arrival date in the breeding area is less steeper than the passage date in the Mediterranean area. This point might deserve a short discussion and some references (please see below).

Both, C. (2010). Flexibility of timing of avian migration to climate change masked by environmental constraints en route. Current Biology, 20(3), 243-248.

Jonzén, N., Lind´en, A., Ergon, T., Knudsen, E., Vik, J.O., Rubolini, D., Piacentini, D., Brinch, C., Spina, F., Karlsson, L., Stervander, M., Andersson, A., Waldenstr¨om, J., Lehikoinen, A., Edvardsen, E., Solvang, R. & Stenseth, N. C. (2006). Rapid advance of spring arrival dates in long-distance migratory birds. Science 312, 1959–1961.

Bitterlin, L. R., & Van Buskirk, J. (2014). Ecological and life history correlates of changes in avian migration timing in response to climate change. Climate Research, 61(2), 109-121.

We added a sentence to acknowledge this (l. 302-304).

LL 390-391. A very important study to be cited here is: Dunn, P. O., & Møller, A. P. (2014). Changes in breeding phenology and population size of birds. Journal of Animal Ecology, 729-739.

We added this reference.

See also the attached file.

Submitted filename: Response to reviewers revision.docx

Click here for additional data file.

8 Sep 2020

Recent phenological shifts of migratory birds at a Mediterranean spring stopover site: species wintering in the Sahel advance passage more than tropical winterers

PONE-D-20-09340R2

Dear Dr. Maggini,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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Kind regards,

Roberto Ambrosini, Ph.D.

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

10 Sep 2020

PONE-D-20-09340R2

Recent phenological shifts of migratory birds at a Mediterranean spring stopover site: species wintering in the Sahel advance passage more than tropical winterers

Dear Dr. Maggini:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

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Thank you for submitting your work to PLOS ONE and supporting open access.

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on behalf of

Dr. Roberto Ambrosini

Academic Editor

PLOS ONE