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Limited potential for bird migration to disperse plants to cooler latitudes

Abstract

Climate change is forcing the redistribution of life on Earth at an unprecedented velocity1,2. Migratory birds are thought to help plants to track climate change through long-distance seed dispersal3,4. However, seeds may be consistently dispersed towards cooler or warmer latitudes depending on whether the fruiting period of a plant species coincides with northward or southward migrations. Here we assess the potential of plant communities to keep pace with climate change through long-distance seed dispersal by migratory birds. To do so, we combine phenological and migration information with data on 949 seed-dispersal interactions between 46 bird and 81 plant species from 13 woodland communities across Europe. Most of the plant species (86%) in these communities are dispersed by birds migrating south, whereas only 35% are dispersed by birds migrating north; the latter subset is phylogenetically clustered in lineages that have fruiting periods that overlap with the spring migration. Moreover, the majority of this critical dispersal service northwards is provided by only a few Palaearctic migrant species. The potential of migratory birds to assist a small, non-random sample of plants to track climate change latitudinally is expected to strongly influence the formation of novel plant communities, and thus affect their ecosystem functions and community assembly at higher trophic levels.

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Fig. 1: Location of the 13 European seed-dispersal networks we studied, and network with bird–plant interactions in relation to bird migration.
Fig. 2: Seed-dispersal interactions of plants with migratory birds in relation to southward and northward migration and Mediterranean or temperate biome.
Fig. 3: Relevance of Palaearctic and Afro-Palaearctic migratory birds dispersing seeds during their southward and northward migration in Mediterranean and temperate communities.

Data availability

All data used in the analyses are available through the Dryad Digital Repository (https://doi.org/10.5061/dryad.15dv41nx3). The dated phylogeny of seed plants (Spermatophyta) used to obtain our phylogenetic tree is available through GitHub (https://github.com/FePhyFoFum/big_seed_plant_trees/releases). Data on bird body weight used for size classification (Supplementary Fig. 2) were obtained from EltonTraits 1.0 available through Figshare (https://doi.org/10.6084/m9.figshare.c.3306933).

Code availability

The R scripts used to generate all results and figures are available through the Dryad Digital Repository (https://doi.org/10.5061/dryad.15dv41nx3).

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Acknowledgements

The ‘Molecular Ecology Laboratory’ (LEM–EBD–CSIC; ISO9001:2015 and ISO14001:2015 certifications) and the ‘Research Unit of Biodiversity’ (UO–CSIC–PA) provided logistical support for molecular analyses. We thank L. Viesca and E. Cires for laboratory assistance, and J. M. Varela for the bird illustrations. Barcoding data were obtained within an Individual Fellowship from the Marie Sklodowska-Curie Actions (H2020-MSCA-IF-2014-656572: MobileLinks) and supported by a GRUPIN grant from the Regional Government of Asturias (IDI/2018/000151). ‘King Jaume I’ awarded to A.T. supported data collation during two postdoctoral contracts. J.P.G.-V. is supported by a Spanish ‘Ramón y Cajal’ fellowship (RYC-2017-22095) and a grant from the Spanish MICINN (PID2019-104922GA-I00/AEI/10.13039/501100011033). B.R. is supported by a Spanish ‘Juan de la Cierva Incorporación’ fellowship (IJCI-2017-33475). R.H.H. is funded by the Portuguese Foundation for Science and Technology (UID/BIA/04004/2020). B.I.S. is supported by a Royal Commission for the Exhibition of 1851 Research Fellowship. W.J.S. is funded by Arcadia.

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Authors

Contributions

J.P.G.-V. conceived the study. J.P.G.-V., J.A., J.M.A., R.S.B., T.B., G.E.-Á., N.F., D.G., J.C.I., P.J., P.K., W.J.S. and E.V. obtained data of seven new seed-dispersal networks within the EU project MobileLinks. J.M.A. and J.C.I. also conducted the molecular analyses for these networks. L.P.d.S. and R.H.H. provided data of one unpublished network. P.J. provided data of two published networks. B.R., J.P.G.-V. and A.T. gathered data on fruiting phenology and bird migrations; J.P.G.-V., B.R., J.A. and B.I.S. analysed the data; J.P.G.-V. wrote the first manuscript draft, and all authors worked on the final version.

Corresponding author

Correspondence to Juan P. González-Varo.

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Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature thanks Christiaan Both, Barnabas Daru, David Inouye, Duarte Viana and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Extended data figures and tables

Extended Data Fig. 1 Conceptual diagrams showing directional patterns of long-distance seed dispersal by migratory birds and phenological overlaps between seed-dispersal periods and bird migrations.

a, Yellow and black arrows denote long-distance seed dispersal within and beyond the current range of a plant species, respectively. Seed dispersal mediated by birds migrating south (left), non-migrating birds (centre) and birds migrating north (right). The colour gradient from red to blue represents a climatic gradient from warmer to cooler latitudes (from south to north in the Northern Hemisphere), respectively. In the diagram on the right, seed dispersal within the range is necessary for warm-adapted populations to colonize cooler areas that are warming owing to climate change, whereas seed dispersal beyond the range is necessary for range shifts. b, Three hypothetical examples of phenological overlap between the seed-dispersal period of plant species i and bird species j while the bird migrates northwards (top), southwards (middle) or during both migrations (bottom). The examples include a wintering migrant with a winter–spring fruiting plant (top); a summer migrant with a summer–autumn fruiting plant (middle); and a transient migrant with an autumn–winter fruiting plant (bottom). In some cases, there is also phenological overlap during non-migration periods. More details on phenological overlaps in relation to the migratory strategy of birds are provided in Supplementary Fig. 3.

Extended Data Fig. 2 Estimated interaction frequencies of plant species within each study network with birds migrating northwards, southwards or not migrating.

Blue, interactions during northward migration; red, interactions during southward migration; grey, non-migration interactions. Each panel represents a seed-dispersal network. The left column of panels includes Mediterranean networks, whereas the right column includes temperate networks. DE, Germany; ES, Spain; IT, Italy; PL, Poland; PT, Portugal; UK, United Kingdom.

Extended Data Fig. 3 Variables of the seed-dispersal phenology across the phylogenetic tree of plants.

Phylogenetic signal was tested in plant-species means across networks in start and end dates (Dstart and Dend), as well as in length (Dlength = Dend – Dstart) of the seed-dispersal period (n = 81 plant species) by means of Pagels’ λ, as described in ‘Phylogenetic signal in plants’ in ‘Statistical analyses’ (Methods). The three phenological variables showed significant phylogenetic signal (Dstart, λ = 0.800, P = 0.0103; Dend, λ = 0.781, P = 0.0015; and Dlength, λ = 0.419, P = 0.0343). To test for phylogenetic signal, we previously calculated the species-level means for Dstart, Dend and Dlength across bioclimates (Extended Data Fig. 6). For this reason, we assessed the amount of variance in these phenological variables that is accounted for by bioclimate, as compared to that accounted for by species through linear-mixed models (LMMs) that included ‘bioclimate’ as fixed factor and ‘plant species’ as random factor to account for the repeated measures per species. Bioclimate accounted for only a minor fraction of variance (1–3%) in Dstart, Dend and Dlength, as shown by the marginal R2 values (variance explained by fixed effects; R2LMM(m) = 0.028, 0.01 and 0.023, respectively). By contrast, the high conditional R2 values (variance explained by both fixed and random effects; R2LMM(c) = 0.780, 0.845 and 0.643, respectively) indicated that plant species accounted for most variance in the three phenological variables. LMMs were fitted with the R package package lme4 (v.1.1-19)105.

Extended Data Fig. 4 Number of migratory bird species interacting with plants during migration per network in relation to migration direction and biome.

Large dots and bars denote means ± 95% confidence intervals estimated by a GLMM, whereas circles denote values for each seed-dispersal network (n = 26 observations, 13 networks × 2 directions). Only migration direction had significant effects on the number of migratory bird species interacting with plants during migration in the GLMM (Poisson family and log-link function) testing the effects of migration direction (Wald χ2 = 11.08, P = 0.0009), biome (Wald χ2 = 0.17, P = 0.6789) and their interaction (Wald χ2 = 0.02, P = 0.8921). Model estimates ± s.e.: intercept = 2.297 ± 0.156; direction (northward) = –0.500 ± 0.208; biome (temperate) = –0.091 ± 0.215; direction (northward) × biome (temperate) = 0.039 ± 0.288; southward and Mediterranean were used as the reference categories (intercepts) for the factors direction and biome, respectively. A mean of 9.5 bird species per community dispersed plants during their southward migration, but only 5.9 species did so during the northward migration.

Extended Data Fig. 5 Individual and cumulative bird species strengths accumulated across seed-dispersal subnetworks.

a, Bird species strength accumulated across seed-dispersal subnetworks between plants and birds migrating southwards or northwards, and in Mediterranean and temperate biomes; species strength quantifies the relevance of a bird species across the entire fleshy-fruited plant community104 (n = 24 species). Some bird species have stacked values from several subnetworks, whereas other species participated only in a single subnetwork. b, The cumulative species strength across the southward and northward subnetworks were significantly correlated in the Mediterranean (Kendall’s τ = 0.396, P = 0.0129) and the temperate biome (τ = 0.588, P = 0.0006), indicating that bird species generally display a proportional role in both migrations. However, the cumulative species strength in the Mediterranean and temperate biome were not correlated, neither across the northward (τ = 0.276, P = 0.1089) nor across the southward subnetworks (τ = 0.263, P = 0.0764) (correlation between left and right panels in a). These results indicate discordance between biomes in the identity of bird species contributions to community-wide seed dispersal during each migration. Pearson’s r yielded qualitatively similar results, with higher coefficient values in the significant correlations (r = 0.946 and 0.847).

Extended Data Fig. 6 Bioclimate-level plant phenology from several sources.

Subset of 16 out of the 81 plant species present in the study networks illustrating how, in many cases, we obtained data on seed-dispersal phenology from several sources for the same plant species–bioclimate combination. Colour codes denote different data sources. A vertical grey line divides the calendar year.

Extended Data Table 1 Characteristics of the European seed-dispersal networks that we studied
Extended Data Table 2 List of bird and plant species of the 13 study networks
Extended Data Table 3 Significance of the fixed factors migration direction and biome, and their interaction, in GLMMs testing effects on seed-dispersal interactions of plants with migrating birds
Extended Data Table 4 Significance of the fixed factors migration direction and biome, and their interaction, in GLMMs testing effects on the proportion of migratory bird species that were Palaearctic migrants, and in the network-level frequency of seed-dispersal interactions with Palaearctic migrants

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Supplementary Information

This file contains the Supplementary methods, Supplementary Discussions 1-2, Supplementary Figures 1-7 and Supplementary References.

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González-Varo, J.P., Rumeu, B., Albrecht, J. et al. Limited potential for bird migration to disperse plants to cooler latitudes. Nature 595, 75–79 (2021). https://doi.org/10.1038/s41586-021-03665-2

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