Abstract
Naturally occurring stable isotope ratios in animal tissues allow estimation of species trophic position and ecological niche. Measuring multiple isotopes of migratory species along flyway bottlenecks offers the opportunity to sample multiple populations and species whose tissues carry information at continental scales. We measured δ2H, δ18O, δ13C, δ15N in juvenile feathers of 21 bird species captured at a migratory bottleneck in the Italian Alps. We examined if trends in individual isotopes reflected known migratory strategies and whether dietary (δ13C–δ15N) and spatially-explicit breeding origin (δ2H–δ18O) niche breadth (NB) differed among long-distance trans-Saharan (TS), short-distance (IP) and irruptive (IR) intra-Palearctic migrants, and whether they correlated with reported populations long-term trends. In both TS and IP groups, species δ2H declined with capture date, indicating that northern populations reached the stopover site later in the season, following a Type-I migration strategy. Values of δ2H indicated that breeding range of TS migrants extended farther north than IP and IR migrants. The breeding season was longer for IP migrants whose δ13C and δ15N values declined and increased, respectively, with time of capture. Average species dietary NB did not differ among migratory groups, but TS migrants displayed wider breeding origin niches, suggesting that long-distant migration is linked to broader ecological niches. Isotope origin NB well reflected species geographic range extent, while dietary NB did not correlate with literature accounts of species’ diet. We found no relationship between species breeding NB and population trends in Europe, suggesting that conditions in the breeding grounds, as inferred by stable isotopes, are not the only determinant of species’ long-term persistence. We demonstrate that ringing activities and isotopic measurements of passerines migrating through a bottleneck represents a unique opportunity to investigate large-scale life-history phenomena relevant to conservation.
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Introduction
The concept of species’ niche is a fundamental pillar of ecological science1,2,3, but remains challenging to quantify empirically. The challenge is particularly acute in the case of long-distance migratory birds due to the shifts in habitat use and distribution throughout their life cycles. Yet, habitat conditions in the breeding, stop-over and wintering grounds profoundly influence individual fitness and demography of migratory populations. Long-distance migrants are showing rapid population declines and appear at greater risk of extinction compared to residents4,5,6. Therefore, assessing niche parameters and differences among migratory groups can help in understanding the drivers shaping migration strategies and setting conservation actions.
Migratory pathways of multiple species often overlap at stopover sites, which can represent bottlenecks, or passage points, causing high spatio-temporal concentration of many individuals and species from different migratory systems7,8,9. Therefore, estimating niche parameters of individuals intercepted along migratory flyways may be a valuable and cost-effective approach to include multiple species potentially conveying information from large, continental scale, breeding areas9,10,11.
Ecological niches of species can be approximated using measurements of naturally occurring stable isotope ratios in their tissues. Such isotopic niches can be used to empirically quantify the realised niche dimensions of species12,13, since stable isotope measurements in animal tissues provides a time-integrated average of many feeding events14. In particular, stable isotope ratios of carbon (δ13C) and nitrogen (δ15N) have been used to represent the “dietary niche” of an organism because they reflect reliance on different primary producers and trophic level, respectively. Although, the dietary niche breadth represented by δ13C and δ15N reflects the range in isotope values of dietary inputs in any given area15,16, the isotopic niche space produced is a potentially powerful means of deriving information on diets of migratory birds from broad catchment areas13,17.
Similarly, isotopic values of hydrogen (deuterium; δ2H) and oxygen (δ18O) are linked to isotopic values in environmental waters that can show predictable spatial patterns or isoscapes at continental scales18. Therefore, tissue δ2H and δ18O values can be used to represent a spatially-explicit “origin niche” of bird species19. Although the meteoric relationship predicts a strong correlation between water δ2H and δ18O, this strong relationship tends to break down in consumer tissues within food webs due to the fact that oxygen in tissues, unlike hydrogen, can be derived from air as well as diet and drinking water. Moreover, metabolic pathways leading to oxygen incorporation in proteins differ from those involving hydrogen20,21. The net result is that the two isotopes tend to be poorly correlated in feathers11. As such, values of δ2H and δ18O could be considered independent in the analyses of feathers and their combined isotopic space would be highly associated with the geographic origins where feathers were grown22.
The use of multiple isotopes in animal tissues has allowed ecologists to estimate trophic niche breadths of different species or individuals in populations12,23, and the geographic origin of migratory species24,25. These studies have provided insight into trophic relationships in communities26,27,28 as well dietary specialisation12 and migratory pathways of declining bird species5,29. Due to logistic and economic constraints, most studies measuring both dietary and origin isotope niches have focused on single species or local populations and communities but see10,30,31. However, examining multiple isotope niches at migratory bottlenecks offers the unique opportunity to quantify and compare niche parameters among several bird species that evolved different migratory behaviours.
In this study, we measured multiple isotopes in the juvenile feathers (remiges and/or retrices) of approximately 800 individuals from 48 species of European passerines captured during the post-breeding migration (August–October) at an Alpine migratory bottleneck over the Italian Alps. Metabolically inert tissues such as feathers show an isotopic composition that reflects the environment during their formation. As a consequence, bird feathers grown in the nest represent “remote carriers” of isotopic information from the breeding grounds32, since many species retain juvenile plumage during subsequent migration and overwintering. In particular, we examined whether dietary (δ13C–δ15N) and origin (δ2H–δ18O) niche breadths (NB) differed among species belonging to the trans-Saharan (TSM), intra-Palearctic (IPM), and irruptive intra-Palearctic (IRM) migratory systems, and the extent to which feather stable isotope values reflected known migratory patterns.
For both TSM and IPM groups, we expected northern populations to reach the autumn Alpine passage later in the season than populations breeding at lower latitudes. According to the deuterium precipitation isoscape in the Palearctic18,19, this would result in a negative relation between arrival date and δ2H for each species, as also observed in Neotropical species adopting a Type-I migration strategy whereby southern populations precede northern ones or as “chain migrants”9.
Since IPM species display a longer breeding season (2–3 clutches) compared to TSM (1–2 clutches), we also compared temporal variation in δ13C and δ15N for each species to examine changes in the availability of main food sources (e.g. larvae to adult insects) during the year of sampling.
Long-distance migration is thought to have evolved primarily in species able to utilise multiple habitat types33,34,35, which are encountered en route and in wintering areas. More generally, if migratory connectivity occurs at large scales, it could favour the selection for generalist traits. As such, species migration distance is expected to be directly related to their niche breadth. Although intuitively appealing, this hypothesis has received limited empirical support so far34,36,37. Here, we specifically examine how migratory distance was related to the origin niche breadth (δ2H–δ18O). We test the hypothesis that long-distance migrants such as TSM species, display broader niches than IPM and IRM species.
Because the relation between isotope niche measures and other estimates of species niche are still poorly understood23, we also examined whether our measures of dietary and origin isotope niches matched diet and climatic niche breadth derived from the literature and species range maps35. While we expected estimates of spatially-explicit isotope origin niche to accord with species range maps, isotope dietary niche breadth is unlikely to match literature data. This is because diet isotopic dimensions largely depend on the inherent isotopic variance of the resources23, and thus may not adequately reflect the diversity of individual food items in the diet (as reported in the literature), but rather the isotopic diversity of used resources.
Lastly, we assessed whether species isotope niche breadths in the breeding range were related to their long-term population trends as reported in the literature. This is of particular importance for long-distance migrants that show rapid population declines4,5. If species with narrow isotope niches systematically displayed negative population trends, it would indicate that conditions at the breeding grounds are key for the long-term persistence of species.
Results
Over the four years of sampling at the two ringing stations, feathers were collected for isotopic analysis from more than 800 individuals of 48 passerine species. After excluding species with less than 15 individuals (see “Methods” section), we included isotope data from 715 individuals of 21 species (Table S1). These belonged to the trans-Saharan (7 species; 241 individuals), intra-Palearctic (11 species; 335 individuals) and irruptive (3 species; 91 individuals) migratory systems. Overall distribution of species over isotope space is shown in Figs. 1 and 2. Migratory phenology of each species during the post-breeding passage is shown in Fig. S1 (Supplementary Material), where the temporal patterns in the number of species captured is also shown.
Temporal changes in δ2H (reflecting species breeding latitude) supported the hypothesis that both TSM and IPM groups display a Type-I (chain) migration, whereby northern populations (with lower δ2H values) reached the Alpine passage later in the season (Fig. 3). This pattern appeared consistent among species in each group, with a significant effect of capture day in the lme model (p < 0.01 for both groups). Mean δ2H values were evidently lower for TSM, indicating that species in this migratory group tend to breed at higher latitudes than IPM. No temporal trend in δ2H was observed in IRM species.
A trend in δ15N was evident for IPM and IRM species with a positive effect of capture day (lme p < 0.01). This trend was not observed in TSM, which displayed slightly higher mean δ15N values (Fig. 3). Similarly, a significant negative trend in δ13C was observed in IPM (p < 0.01), which was not significant in either TSM and IRM species. Figure 3 also shows that most TSM species reached the capture site by day 280, whereas the season appeared longer for IPM and IRM. The difference in phenology is also clear from Fig. S1.
Average species dietary isotopic NB did not differ significantly among migratory groups (Fig. 4). Conversely, the average isotopic origin niche was significantly broader for TSM, about 30% broader than IPM (GLS model; p = 0.03). However, there was relatively large variation in origin NB within TSM. IRM displayed a much narrower origin NB (Fig. 4). Excluding the apparent outliers from the analysis of dietary NB (δ13C–δ15N; Regulus regulus and Delichon urbicum), provided qualitatively similar results.
In addition, migration distance was related to the breadth of species origin niche, although there was considerable variation at larger distances (Fig. 5; GLS; p = 0.01). No relationship was observed between dietary isotopic NB and migration distance (Fig. S2).
We compared our estimates of species dietary and origin isotopic niche with those recently derived from species distributional data. We found that the origin NB well matched measures from range maps (Fig. 6), with a positive linear correlation (p = 0.02). In addition, climate niche breadth derived from range maps well reflected the upper distribution of the empirical isotope origin niche. This is evident from the significant quantile regression at q = 0.8 (p < 0.01). Conversely, the dietary isotopic NB was not related to diet specialisation, as derived from the literature.
Finally, we appraised whether long-term population trends were related to the empirical isotope niches. Neither dietary nor origin isotopic niche breadth were related to species population trends as reported in the PECBMS portal (Fig. S3).
Discussion
We used juvenile feathers of multiple bird species intercepted along an autumn migratory flyway as ‘remote carriers’ of isotope niche information from Western Palearctic breeding areas. This allowed quantifying niche parameters from species that evolved different migratory strategies. In addition, despite potential confounding factors related to variance in local isotopic baselines, including individuals from different populations and communities allowed the quantification of species niches that were less influenced by local biotic interactions (e.g. competition), and likely more representative of the realised niche dimensions of the species.
Our results generally supported our initial hypotheses, but also revealed a poor association between isotope niche dimensions and literature-derived niche parameters and long-term population trends.
Temporal trends in feather δ2H indicated that individuals breeding at higher latitudes (displaying lower δ2H values) reached the sampling locations later in the season, with patterns that appeared consistent among species and across the two major migratory groups (TSM, IPM). This type of migration, often called Type I (as opposed to Type-II, whereby northern populations leap-frog southern populations during migration), has also been observed across a range of Nearctic-Neotropical migrants9,38, and appears common in Afro-Palearctic migrants as well39,40. Different migration timing of conspecific populations contributes to limit competition among individuals and likely occurs at the species level too. Assessing temporal segregation in the use of migratory stopover helps identify the species most likely to co-occur and compete locally for resources. In our study site, a few species showed complete segregation (Fig. S1), but high overlap was otherwise evident with up to nine migratory species captured in a single day. Bottlenecks can indeed concentrate large numbers of individuals and species during a short period, which not only heightens intra- and inter-specific competition, but also increases vulnerability to localised events and disturbance. The identification and conservation of migratory stopover and bottlenecks are therefore key for the persistence of many declining populations7,8,9.
Temporal trends observed in both δ15N and δ13C in IPM could be explained by different non-mutually exclusive mechanisms. For instance, the lower latitude breeding range of IPM, as well as IRM (compared to TSM), implies that early captures were dominated by individuals from the Alpine/central-Europe/Carpathian areas at high elevations. This could be associated with higher δ13C19 also due to lower precipitation compared to northern Europe41. Similarly, it is also possible that the extent of anthropogenic nitrogen input from agriculture is lower in mountainous regions, which could contribute to lower δ15N in early captures. It is known, in fact, that anthropogenic sources such as fertilisers can alter and mostly increase nitrogen isotopic baseline values23.
Alternatively, seasonally rising values of δ15N could be associated with the increased availability of adult insects (as opposed to larvae or other arthropods with lower δ15N values) as the longer breeding season of IPM progresses. Conversely, the shorter season of TSM and their strictly insectivorous diet would result in more seasonally stable δ15N values.
We found that species breeding origin niche was, on average, broader in long-distance trans-Saharan compared to intra-Palearctic migrants. Long-distance migration is generally thought to have evolved from ancestor species with broad habitat niches: individuals able to exploit a wider range of conditions during migration or at wintering grounds should be selectively advantaged over more specialised ones33,34,35. Empirical support for this hypothesis is limited36,42,43, and our data thus provide some additional evidence. However, the link between niche breadth and migration patterns remains unclear, with some evidence suggesting the opposite view that narrower habitat or diet niche may have favoured long-distance migrations44, because specialists are forced to leave an area when conditions become unfavourable or resources scarce. Yet, our data do not show any correlation between migration distance and dietary niche breadth, providing no support for this alternative hypothesis. It has to be kept in mind, however, that our estimates of ecological niches reflect the breeding diets of species (i.e. isotopes from juvenile feathers grown at nest), and the inclusion of information from wintering grounds would have provided a more complete and likely different picture. This would require measuring isotope ratios in body tissues with different turnover or growth rates45, or collecting feathers grown in winter29. However, for most passerine species, information on wintering locations is still limited, especially for the Afro-Palearctic migration system46,47. Similarly, the extent to which migratory species track their climate and habitat niche between breeding and wintering grounds is poorly understood and likely to vary among species37,47. Most assessments of seasonal niche shifts during migration relied on large-scale climatic and land-use data37,48, while those employing tissue isotopes are rare and mostly focussed on a few key species to appraise migratory connectivity10,45,49. Therefore, it is difficult to evaluate whether and to what extent our estimates of isotope niche breadth would have differed had we included wintering isotope signals.
We used recently published data from Reif et al.35 to examine the extent to which isotope niches from our sampled populations reflected diet specialisation and climate niche breadth reported at the species level. As expected, dietary isotopic niche did not match the breadth or diversity of consumed food items reported in the literature. This further supports the notion that the breadth of dietary isotope niche reflects the isotopic variance of the resources and should not be considered synonymous with species diet23. Conversely, estimates of spatially-explicit breeding origin niche correlated significantly, albeit weakly, with literature data. In particular, measures of climatic niche from range maps appeared to better predict the upper distribution (quantile: 0.8) of our isotope niche, rather than its central response. A possible interpretation is that niche estimates derived from range maps necessarily reflect the maximum expected value for a given population. In other words, if we assume that a correlation exists between spatially-explicit origin niche inferred from isotope and range maps, any sampled populations should display isotope niches that are either equal or narrower than those derived from species full range maps. This provides additional evidence that species bi-dimensional δ2H–δ18O isotope space is a good proxy of their geographic and climatic niche dimensions30.
Among the key motivations for appraising niche requirements of migratory species, is that their populations appear to be declining more rapidly than residents4,5,50,51. The mechanisms underpinning these trends are still unclear and we examined whether narrow isotope breeding niches were associated with stronger population declines. We found no correlation between either dietary or origin breeding niche and long-term population trends as reported in the Pan European Common Bird Monitoring Scheme. This is not surprising as there is increasing evidence that environmental conditions and dynamics in non-breeding areas are key for the long-term persistence of populations50,52,53. In particular, habitat change and degradation in tropical wintering areas appear to be a major cause of decline in migrant species. As the conditions in wintering grounds carry-over to influence breeding success54,55, quantifying both breeding and wintering niche parameters would provide insight not only on basic ecological questions such as the degree of niche tracking, but also on conservation requirements of long-distance migrants45.
We used multiple stable isotopes to quantify and compare ecological niche parameters between short- and long-distance migrants. We showed that post-breeding migratory bottlenecks, such “Bocca di Caset” and “Passo del Brocon” in the Italian Alps, not only represent important stopovers for many migrants of the Western flyway40, but also strategic natural laboratories to examine migratory patterns across multiple species. However, not every species or populations are equally likely to use these locations as stopover. For instance, some central-European populations could fly over the Alps during the first migratory flight without stopping. The extent to which the potential selectivity of our study area influenced the results depends on the heterogeneity in isotope profiles within populations, which, however, can be large in some cases55,56.
Our results illustrate that long-distance trans-Saharan migrants, mostly breeding at higher latitudes than intra-Palearctic migrants, reach the migratory stop-over sooner. This is in line with the notion that early departure allows trans-Saharan migrants to reach the Sahel zone at the peak of vegetation greenness, when feeding conditions are optimal57,58. Moreover, in both migratory groups, the onset of breeding for northern populations appeared delayed, likely due to climatic constraints, so that the timing of migration was proportionally shifted later in the season. The delayed timing of northern populations can apparently carry over to the entire annual cycle39, and likely contributes to limit intra-specific competition. This type of migration pattern appears fairly common in many Nearctic-Neotropical migrants too9,38.
Our data also provide some support to the hypothesis that broad ecological niches are linked to long-distance migration, although this was only evident for the breeding origin niche dimensions, and requires further testing.
The use of multiple isotope ratios in animal tissues has allowed the quantification of both dietary and spatially-explicit niche aspects. However, the relation between the isotopic ecological niche and other descriptors of species niche (e.g. based on feeding habits, distribution patterns), or conservation status remains vague23,30. Here, we found that origin isotopic niche was consistent with the climatic range extent of the species, illustrating how δ2H and δ18O measurements can provide insight into the bio-climatic and geographic niche dimensions. However, the breadth of isotope niches was not related to the long-term population trends of the species at the European scale. Appraisal of the complete multi-seasonal niche requirements of long-distance migrants is therefore needed to link ecological information to conservation actions for these declining species.
Methods
Feather sampling
From 2010 to 2013, juvenile wing and tail feathers grown in the nest59 from 807 migratory birds belonging to 48 passerine species were sampled at the ‘Bocca di Caset’ and ‘Passo del Brocon’ ringing stations of MUSE (Province of Trento, Italy, 10° 41′ E, 45° 51′ N, 1605 m a.s.l. and 11° 68′ E, 46° 11′ N, 1720 m a.s.l., respectively) in the central Italian Alps during post-breeding migration (August to the end of October). The study is part of the long-term post-breeding monitoring project ‘Progetto Alpi’60. We only included species with at least 15 sampled individuals (median individuals per species = 26) to provide a representative measure of species isotopic niches. The remaining species were represented by a median of 3 individuals and were excluded (Fig. S4). Migratory species pass through the Italian Alps at different times during autumn migration60. Three migratory groups were considered: long-distance trans-Saharan migrants (TSM), which are fully migratory and leave their breeding ranges to winter in sub-Saharan Africa; short-distance intra-Palaearctic migrants (IPM), which can be fully or partially migratory and which have their breeding and wintering ranges within the Western Palaearctic; irruptive intra-Palaearctic migrants (IRM), which are partial migrants and residents, but show marked invasive and nomadic movements during non-breeding seasons. Date of capture was also recorded for each individual.
Stable isotope analysis
Values of δ2H, δ18O, δ13C, δ15N were measured for each individual feather. It was possible to determine all four isotope ratios in the majority of individuals. Feathers were first washed in a solvent mixture (diethyl ether-methanol 2:1) prior to analysis61. Simultaneous determination of δ13C and δ15N was accomplished using a Vario Isotope Cube isotope ratio mass spectrometer (Elementar, Germany). The δ2H and δ18O values were determined through pyrolysis combustion using a TC/EA (Thermo Finnigan, Bremen, Germany) interfaced with a Delta Plus XP (Thermo Finnigan, Bremen, Germany) continuous-flow isotope-ratio mass spectrometer. Pyrolysis was carried out at 1450 °C in a glassy carbon column. The helium carrier flow was 110 ml/min, the GC column was a 1.2 m long molecular sieve 5A, at 110 °C. Isotope ratios were expressed in δ-notation against V-PDB (Vienna-Pee Dee Belemnite) for δ13C, Air for δ15N, V-SMOW (Vienna-Standard Mean Ocean Water) for δ2H and δ18O. Isotopic values of δ2H were calculated using the comparative equilibration approach62,63. Based on the keratin standards CBS (δ2H − 197 ‰, δ18O = + 3.8 ‰) and KHS (− 54.1 ‰, δ18O = + 20.3 ‰). Values of δ13C and δ15N were calculated against working in-house standards (casein and wheat), which were themselves calibrated against international reference materials using multi-point normalisation: fuel oil NBS-22 (IAEA International Atomic Energy Agency, Vienna, Austria; − 30.03 ‰) and sugar IAEA-CH-6 (− 10.45 ‰) for δ13C, L-glutamic acid USGS 40 (− 26.39 ‰ and − 4.5 ‰ for δ13C and δ15N), hair USGS 42 (δ15N = + 8.05 ‰ and δ13C = − 21.09 ‰) and USGS 43 (δ15N = + 8.44 ‰ and δ13C = − 21.28 ‰) for 13C/12C and 15N/14N. Values of δ13C were expressed versus V-PDB on a scale normalised against the two reference materials LSVEC (− 46.6 ‰) and NBS 19 (+ 1.95 ‰)64. Values of δ15N were expressed versus Air-N2 on a scale normalised using the two reference materials IAEA-N-1 and USGS32, with consensus values of + 0.4 ‰ and + 180 ‰64. Method uncertainty (calculated as one standard deviation) was 0.1 ‰ for δ13C, 0.2 ‰ for δ15N, 0.3 ‰ for δ18O and 2 ‰ for δ2H.
Data analysis
We gathered information on migratory behaviour and distance for each bird species from the literature65. Migration distance was estimated as the distance between the breeding and wintering areas. Specifically, distance was estimated as the mean of the two latitudes during breeding minus the mean of the two latitudes during winter66.
To compare empirical estimates of dietary and origin isotopic niche breadth with literature data, we used recently published measures of diet specialisation and climate niche breadth that were derived from literature data and breeding range maps of European birds35. Diet specialisation was expressed as the coefficient of variation in the presence/absence of eight food types in the diet of each species (foliage, fruit, grain, insects, other invertebrates, terrestrial vertebrates, water vertebrates, carrion). Climate niche breadth was measured by overlying the breeding range map of each species to climatic data and calculating the covered temperature range35.
Information on long-term population trends for each species at the European scale was gathered from the Pan European Common Bird Monitoring Scheme (PECBMS) (https://pecbms.info/trends-and-indicators/species-trends/).
Dietary isotopic niche breadth (NB) was expressed as the Bayesian Standard Ellipse Area corrected for small sample size (SEAc) using the isotopic space defined by δ13C–δ15N. Similarly, spatially-explicit origin NB was expressed as SEAc from the δ2H–δ18O space. The SIBER R-package was used for these calculations30,67.
Differences in NB among migratory groups were examined using generalised least squares (GLS) allowing the variance to differ among groups (with varIdent function in R). Seasonal trends in δ2H, δ13C and δ15N within each migratory group were assessed using linear mixed-effect models including species as random factor to account for different isotope values and trends across species. We used the lme function in R allowing both intercept and slope to differ among species. To examine if origin NB was related to migration distance, we used GLS to regress the mean NB values for each species (across all measured individuals) against the estimated migration distance, allowing the variance to differ among species (with varFixed).
Although migration timing can vary within species depending on age and sex, our analyses only included juveniles born in the year of sampling, which were likely fed a similar diet regardless of sex. In fact, no particular differences in isotope patterns were observed between male and female for the species that we were able to sex (Figs. S5, S6).
Ethics approval
All experimental procedures including the permission to trap and hold birds in temporary captivity were authorized by the Autonomous Province of Trento (Autorizzazione del Comitato faunistico provinciale n. 549, 17th February 2009; Autorizzazione del Comitato faunistico provinciale n. 608, 21st November 2011) and were carried out in compliance with the current Italian laws regulating scientific research on animals.
All experimental methods, statistical analyses and results were carried out and reported in accordance with the ARRIVE guidelines on animal research.
Data availability
All data used in this study are available in the Dryad repository at: https://doi.org/10.5061/dryad.fn2z34tsk, and will be made publicly available upon acceptance of the manuscript.
Change history
04 November 2021
A Correction to this paper has been published: https://doi.org/10.1038/s41598-021-01429-6
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Acknowledgements
Funding to A.F. was provided by FEM—Fondazione Edmund Mach, Research and Innovation Centre and MUSE—Science Museum of Trento (Accordo di Programma—Provincia Autonoma di Trento). This study complies with the current Italian laws regulating scientific research on animals. The authors gratefully acknowledge G. Bogliani (University of Pavia) and S. Tenan (MUSE), for their suggestions in the early phase of this study, and A. Tonon and L. Ziller for the analytical support, S. Noselli, F. Rizzolli and F. Rossi for field work. Comments from two anonymous reviewers greatly improved the quality of the work.
Funding
Funding to A.F. was provided by FEM—Fondazione Edmund Mach, Research and Innovation Centre and MUSE—Science Museum of Trento (Accordo di Programma—Provincia Autonoma di Trento).
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A.F., P.P. and F.C. conceived and designed the study. P.P. led fieldwork organization. A.F. and P.P. carried out most fieldwork. S.L., P.F. and A.F. analysed the data. S.L., A.F., L.B. and P.F. wrote the main manuscript. All authors reviewed the manuscript and contributed critically to the final draft.
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Franzoi, A., Larsen, S., Franceschi, P. et al. Multidimensional natal isotopic niches reflect migratory patterns in birds. Sci Rep 11, 20800 (2021). https://doi.org/10.1038/s41598-021-00373-9
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DOI: https://doi.org/10.1038/s41598-021-00373-9
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