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Accelerating homogenization of the global plant–frugivore meta-network

Nature volume 585, pages 74–78 (2020)Cite this article

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Abstract

Introductions of species by humans are causing the homogenization of species composition across biogeographic barriers1,2,3. The ecological and evolutionary consequences of introduced species derive from their effects on networks of species interactions4,5, but we lack a quantitative understanding of the impacts of introduced species on ecological networks and their biogeographic patterns globally. Here we address this data gap by analysing mutualistic seed-dispersal interactions from 410 local networks, encompassing 24,455 unique pairwise interactions between 1,631 animal and 3,208 plant species. We show that species introductions reduce biogeographic compartmentalization of the global meta-network, in which nodes are species and links are interactions observed within any local network. This homogenizing effect extends across spatial scales, decreasing beta diversity among local networks and modularity within networks. The prevalence of introduced interactions is directly related to human environmental modifications and is accelerating, having increased sevenfold over the past 75 years. These dynamics alter the coevolutionary environments that mutualists experience6, and we find that introduced species disproportionately interact with other introduced species. These processes are likely to amplify biotic homogenization in future ecosystems7 and may reduce the resilience of ecosystems by allowing perturbations to propagate more quickly and exposing disparate ecosystems to similar drivers. Our results highlight the importance of managing the increasing homogenization of ecological complexity.

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Fig. 1: Altered interaction biogeography in the global plant–frugivore meta-network.
Fig. 2: Shared species and interaction composition across regions in the presence and absence of anthropogenic species introductions.
Fig. 3: Preferential interaction among introduced species within local networks and introduced species impacts on local network modularity.
Fig. 4: Spatiotemporal variation in the prevalence of introduced species and interactions.

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Data availability

All data used in the analyses are available through the Dryad digital data repository (https://doi.org/10.5061/dryad.44j0zpcbx).

Code availability

All scripts that are needed to reproduce the analyses and figures are available through the Dryad digital data repository (https://doi.org/10.5061/dryad.44j0zpcbx).

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Acknowledgements

We thank the many researchers that collected the field data that were used in this analysis. E.C.F. was supported by the National Socio-Environmental Synthesis Center (SESYNC) under funding received from the National Science Foundation DBI-1639145. J.C.S. considers this work a contribution to his VILLUM Investigator project “Biodiversity Dynamics in a Changing World” funded by VILLUM FONDEN (grant 16549).

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Authors and Affiliations

  1. National Socio-Environmental Synthesis Center (SESYNC), University of Maryland, Annapolis, MD, USA

    Evan C. Fricke

  2. Center for Biodiversity Dynamics in a Changing World (BIOCHANGE), Department of Biology, Aarhus University, Aarhus, Denmark

    Jens-Christian Svenning

  3. Section for Ecoinformatics and Biodiversity, Department of Biology, Aarhus University, Aarhus, Denmark

    Jens-Christian Svenning

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  1. Evan C. Fricke
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Contributions

 E.C.F. conceived the study with J.C.S., assembled and analysed data, and wrote the first draft. Both authors designed analyses and revised the paper.

Corresponding author

Correspondence to Evan C. Fricke.

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The authors declare no competing interests.

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Peer review information Nature thanks Mauro Galetti, Thilo Gross 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 Biogeographic compartmentalization measured via meta-network modularity.

Modularity is calculated given species’ module membership based on the regions in which they are native. High modularity values indicate high compartmentalization along biogeographic regions, with distributions of bootstrapped values shown. Blue distribution shows modularity of the native-only meta-network. Red distribution shows modularity of the observed meta-network including introduced interactions. Red dashed line indicates distribution of modularity values for observed meta-networks sampled to have an equivalent number of interactions as in the native-only meta-network. Because this gives similar modularity values as in the observed meta-network, the higher modularity of the native-only meta-network is not explained by a lower number of interactions. Grey dashed line indicates distribution of modularity values for meta-networks simulated if species were homogenized randomly within biomes; this reflects a null expectation for biogeographic compartmentalization given a lack of dispersal barriers.

Extended Data Fig. 2 Beta diversity in species and interactions among local networks.

Relationship between pairwise distances and similarity of species in the community (1 – βS) and interactions (1 – βWN). Points represent 14,849 pairs of local networks and lines represent model fits from generalized additive models. Top row points in blue (a, b) are calculated using only native interactions and bottom row points in red (c, d) are calculated including introduced interactions.

Extended Data Fig. 3 Interaction breadth of species that have established as introduced species versus species that do not appear as introduced species.

For focal plant and animal species, the normalized degree—number of observed partners divided by the number of potential partners—was greater for species that appear as introduced than for species that do not. In a, b, introduced species are those that have been reported as introduced anywhere according to publicly available databases (χ2a = 59.7, d.f. = 1, Pa = 1.1 × 10−14, χ2p = 14.5, d.f. = 1, Pp = 1.4 × 10−4). In c, d, introduced species are those that are recorded in our database within a local network where they are introduced (χ2a = 235.3, d.f. = 1, Pa < 2.2 × 10−16, χ2p = 40.4, d.f. = 1, Pp = 2.1 × 10−10).

Extended Data Fig. 4 Introduced interactions reduce modularity of local networks.

Model estimates from mixed effects quantile regression, using random intercepts by study location. Points (jittered along x axis) show null model-corrected modularity calculated for 395 local networks as the difference between observed modularity and the average modularity of five corresponding networks generated under a null model. Coefficient estimates (±s.e.m.) at the 5th, 50th and 95th percentiles are, for the intercept, β0,5 = –0.050 (±0.005), β0,50 = 0.012 (±0.004), β0,95 = 0.130 (±0.019), and, for the effect of the proportion of introduced interactions, β1,5 = –0.009 (±0.020), β1,50 = –0.029 (±0.016), β1,95 = –0.079 (±0.037).

Extended Data Table 1 Shared network elements (species and interactions) among the 18 regions
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Extended Data Table 2 The probability that the interaction with introduced partners depends on the native or introduced status of focal species
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Extended Data Table 3 GLMMs assessing the differences in the breadth of interaction partners in local networks 
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Extended Data Table 4 Comparison of LMMs that analyse the null-model-corrected modularity of the local network
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Extended Data Table 5 The relationship between the proportion of introduced interaction and both study year and human modification (gHM)
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Extended Data Table 6 Comparison of the portion of the interactions of 410 local networks that are due to species introductions
Full size table

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Fricke, E.C., Svenning, JC. Accelerating homogenization of the global plant–frugivore meta-network. Nature 585, 74–78 (2020). https://doi.org/10.1038/s41586-020-2640-y

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