Extinction, coextinction and colonization dynamics in plant-hummingbird networks under climate change.
Journal
Nature ecology & evolution
ISSN: 2397-334X
Titre abrégé: Nat Ecol Evol
Pays: England
ID NLM: 101698577
Informations de publication
Date de publication:
06 2022
06 2022
Historique:
received:
25
06
2021
accepted:
07
02
2022
pubmed:
30
3
2022
medline:
11
6
2022
entrez:
29
3
2022
Statut:
ppublish
Résumé
Climate-driven range shifts may cause local extinctions, while the accompanying loss of biotic interactions may trigger secondary coextinctions. At the same time, climate change may facilitate colonizations from regional source pools, balancing out local species loss. At present, how these extinction-coextinction-colonization dynamics affect biological communities under climate change is poorly understood. Using 84 communities of interacting plants and hummingbirds, we simulated patterns in climate-driven extinctions, coextinctions and colonizations under future climate change scenarios. Our simulations showed clear geographic discrepancies in the communities' vulnerability to climate change. Andean communities were the least affected by future climate change, as they experienced few climate-driven extinctions and coextinctions while having the highest colonization potential. In North America and lowland South America, communities had many climate-driven extinctions and few colonization events. Meanwhile, the pattern of coextinction was highly dependent on the configuration of networks formed by interacting hummingbirds and plants. Notably, North American communities experienced proportionally fewer coextinctions than other regions because climate-driven extinctions here primarily affected species with peripheral network roles. Moreover, coextinctions generally decreased in communities where species have few overlapping interactions, that is, communities with more complementary specialized and modular networks. Together, these results highlight that we should not expect colonizations to adequately balance out local extinctions in the most vulnerable ecoregions.
Identifiants
pubmed: 35347259
doi: 10.1038/s41559-022-01693-3
pii: 10.1038/s41559-022-01693-3
doi:
Banques de données
figshare
['10.6084/m9.figshare.19071752.v2']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
720-729Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Schemske, D. W. in Foundations of Tropical Forest Biology (eds Chazdon, R. L. & Whitmore, T. C.) 163–173 (Univ. Chicago Press, 2002).
Hooper, D. U. et al. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monogr. 75, 3–35 (2005).
doi: 10.1890/04-0922
Schemske, D. W., Mittelbach, G. G., Cornell, H. V., Sobel, J. M. & Roy, K. Is there a latitudinal gradient in the importance of biotic interactions? Annu. Rev. Ecol. Evol. Syst. 40, 245–269 (2009).
doi: 10.1146/annurev.ecolsys.39.110707.173430
Schweiger, O., Settele, J., Kudrna, O., Klotz, S. & Kühn, I. Climate change can cause spatial mismatch of trophically interacting species. Ecology 89, 3472–3479 (2008).
pubmed: 19137952
doi: 10.1890/07-1748.1
Hegland, S. J., Nielsen, A., Lázaro, A., Bjerknes, A.-L. & Totland, Ø. How does climate warming affect plant–pollinator interactions? Ecol. Lett. 12, 184–195 (2009).
pubmed: 19049509
doi: 10.1111/j.1461-0248.2008.01269.x
Walther, G.-R. Community and ecosystem responses to recent climate change. Philos. Trans. R. Soc. B 365, 2019–2024 (2010).
doi: 10.1098/rstb.2010.0021
Blois, J. L., Zarnetske, P. L., Fitzpatrick, M. C. & Finnegan, S. Climate change and the past, present and future of biotic interactions. Science 341, 499–504 (2013).
pubmed: 23908227
doi: 10.1126/science.1237184
Schleuning, M. et al. Ecological networks are more sensitive to plant than to animal extinction under climate change. Nat. Commun. 7, 13965 (2016).
pubmed: 28008919
pmcid: 5196430
doi: 10.1038/ncomms13965
Bascompte, J., García, M. B., Ortega, R., Rezende, E. L. & Pironon, S. Mutualistic interactions reshuffle the effects of climate change on plants across the tree of life. Sci. Adv. 5, eaav2539 (2019).
pubmed: 31106269
pmcid: 6520021
doi: 10.1126/sciadv.aav2539
Memmott, J., Craze, P. G., Waser, N. M. & Price, M. V. Global warming and the disruption of plant–pollinator interactions. Ecol. Lett. 10, 710–717 (2007).
pubmed: 17594426
doi: 10.1111/j.1461-0248.2007.01061.x
Tylianakis, J. M., Didham, R. K., Bascompte, J. & Wardle, D. A. Global change and species interactions in terrestrial ecosystems. Ecol. Lett. 11, 1351–1363 (2008).
pubmed: 19062363
doi: 10.1111/j.1461-0248.2008.01250.x
Dalsgaard, B. et al. Specialization in plant–hummingbird networks is associated with species richness, contemporary precipitation and Quaternary climate-change velocity. PLoS ONE 6, e25891 (2011).
pubmed: 21998716
pmcid: 3187835
doi: 10.1371/journal.pone.0025891
Dalsgaard, B. et al. Historical climate-change influences modularity and nestedness of pollination networks. Ecography 36, 1331–1340 (2013).
doi: 10.1111/j.1600-0587.2013.00201.x
Memmott, J., Waser, N. M. & Price, M. V. Tolerance of pollination networks to species extinctions. Proc. R. Soc. Lond. B 271, 2605–2611 (2004).
doi: 10.1098/rspb.2004.2909
Kaiser-Bunbury, C. N., Muff, S., Memmott, J., Müller, C. B. & Caflisch, A. The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour. Ecol. Lett. 13, 442–452 (2010).
pubmed: 20100244
doi: 10.1111/j.1461-0248.2009.01437.x
Dáttilo, W. et al. Unravelling Darwin’s entangled bank: architecture and robustness of mutualistic networks with multiple interaction types. Proc. R. Soc. B 283, 20161564 (2016).
pubmed: 27881755
pmcid: 5136579
doi: 10.1098/rspb.2016.1564
Dalsgaard, B. et al. Trait evolution, resource specialization and vulnerability to plant extinctions among Antillean hummingbirds. Proc. R. Soc. B 285, 20172754 (2018).
pubmed: 29563263
pmcid: 5897636
doi: 10.1098/rspb.2017.2754
Gilman, S. E., Urban, M. C., Tewksbury, J., Gilchrist, G. W. & Holt, R. D. A framework for community interactions under climate change. Trends Ecol. Evol. 25, 325–331 (2010).
pubmed: 20392517
doi: 10.1016/j.tree.2010.03.002
Rahbek, C. & Graves, G. R. Multiscale assessment of patterns of avian species richness. Proc. Natl Acad. Sci. USA 98, 4534–4539 (2001).
pubmed: 11296292
pmcid: 31869
doi: 10.1073/pnas.071034898
Rahbek, C. & Graves, G. R. Detection of macro-ecological patterns in South American hummingbirds is affected by spatial scale. Proc. R. Soc. Lond. B 267, 2259–2265 (2000).
doi: 10.1098/rspb.2000.1277
Dalsgaard, B. et al. The influence of biogeographical and evolutionary histories on morphological trait-matching and resource specialization in mutualistic hummingbird–plant networks. Funct. Ecol. 35, 1120–1133 (2021).
doi: 10.1111/1365-2435.13784
Sandel, B. et al. The influence of Late Quaternary climate-change velocity on species endemism. Science 334, 660–664 (2011).
pubmed: 21979937
doi: 10.1126/science.1210173
Scherrer, D. & Körner, C. Topographically controlled thermal-habitat differentiation buffers alpine plant diversity against climate warming. J. Biogeogr. 38, 406–416 (2011).
doi: 10.1111/j.1365-2699.2010.02407.x
Graves, G. R. & Rahbek, C. Source pool geometry and the assembly of continental avifaunas. Proc. Natl Acad. Sci. USA 102, 7871–7876 (2005).
pubmed: 15911769
pmcid: 1142364
doi: 10.1073/pnas.0500424102
IPCC Climate Change 2014: Impacts, Adaptation, and Vulnerability. Part B: Regional Aspects (eds Barros, V. R. et al.) (Cambridge Univ. Press, 2014).
Hoegh-Guldberg, O. et al. in Special Report on Global Warming of 1.5 °C (eds Masson-Delmotte, V. et al.) 175–311 (IPCC, WMO, 2018).
Watson, J. E. M., Iwamura, T. & Butt, N. Mapping vulnerability and conservation adaptation strategies under climate change. Nat. Clim. Change 3, 989–994 (2013).
doi: 10.1038/nclimate2007
Martín González, A. M., Dalsgaard, B. & Olesen, J. M. Centrality measures and the importance of generalist species in pollination networks. Ecol. Complex. 7, 36–43 (2010).
doi: 10.1016/j.ecocom.2009.03.008
Burgos, E. et al. Why nestedness in mutualistic networks? J. Theor. Biol. 249, 307–313 (2007).
pubmed: 17897679
doi: 10.1016/j.jtbi.2007.07.030
Bersier, L.-F., Banašek-Richter, C. & Cattin, M.-F. Quantitative descriptors of food-web matrices. Ecology 83, 2394–2407 (2002).
doi: 10.1890/0012-9658(2002)083[2394:QDOFWM]2.0.CO;2
Thébault, E. & Fontaine, C. Stability of ecological communities and the architecture of mutualistic and trophic networks. Science 329, 853–856 (2010).
pubmed: 20705861
doi: 10.1126/science.1188321
Tylianakis, J. M., Laliberté, E., Nielsen, A. & Bascompte, J. Conservation of species interaction networks. Biol. Conserv. 143, 2270–2279 (2010).
doi: 10.1016/j.biocon.2009.12.004
Grass, I., Jauker, B., Steffan-Dewenter, I., Tscharntke, T. & Jauker, F. Past and potential future effects of habitat fragmentation on structure and stability of plant–pollinator and host–parasitoid networks. Nat. Ecol. Evol. 2, 1408–1417 (2018).
pubmed: 30082735
doi: 10.1038/s41559-018-0631-2
Stouffer, D. B. & Bascompte, J. Compartmentalization increases food-web persistence. Proc. Natl Acad. Sci. USA 108, 3648–3652 (2011).
pubmed: 21307311
pmcid: 3048152
doi: 10.1073/pnas.1014353108
Blüthgen, N., Menzel, F. & Blüthgen, N. Measuring specialization in species interaction networks. BMC Ecol. 6, 9 (2006).
pubmed: 16907983
pmcid: 1570337
doi: 10.1186/1472-6785-6-9
Dormann, C. F. & Strauss, R. A method for detecting modules in quantitative bipartite networks. Methods Ecol. Evol. 5, 90–98 (2014).
doi: 10.1111/2041-210X.12139
Bascompte, J., Jordano, P., Melián, C. J. & Olesen, J. M. The nested assembly of plant–animal mutualistic networks. Proc. Natl Acad. Sci. USA 100, 9383–9387 (2003).
pubmed: 12881488
pmcid: 170927
doi: 10.1073/pnas.1633576100
Rahbek, C. et al. Humboldt’s enigma: what causes global patterns of mountain biodiversity? Science 365, 1108–1113 (2019).
pubmed: 31515383
doi: 10.1126/science.aax0149
Cracraft, J. Historical biogeography and patterns of differentiation within the South American avifauna: areas of endemism. Ornithol. Monogr. 36, 49–84 (1985).
doi: 10.2307/40168278
Hazzi, N. A., Moreno, J. S., Ortiz-Movliav, C. & Palacio, R. D. Biogeographic regions and events of isolation and diversification of the endemic biota of the tropical Andes. Proc. Natl Acad. Sci. USA 115, 7985–7990 (2018).
pubmed: 30018064
pmcid: 6077705
doi: 10.1073/pnas.1803908115
Jønsson, K. A. et al. Tracking animal dispersal: from individual movement to community assembly and global range dynamics. Trends Ecol. Evol. 31, 204–214 (2016).
pubmed: 26852171
doi: 10.1016/j.tree.2016.01.003
McGuire, J. A. et al. Molecular phylogenetics and the diversification of hummingbirds. Curr. Biol. 24, 910–916 (2014).
pubmed: 24704078
doi: 10.1016/j.cub.2014.03.016
Proctor, M., Yeo, P. & Lack, A. The Natural History of Pollination (HarperCollins, 1996).
Simberloff, D. S. & Wilson, E. O. Experimental zoogeography of islands: the colonization of empty islands. Ecology 50, 278–296 (1969).
doi: 10.2307/1934856
Connor, E. F. & Simberloff, D. Species number and compositional similarity of the Galapagos flora and avifauna. Ecol. Monogr. 48, 219–248 (1978).
doi: 10.2307/2937300
Grant, P. R. & Abbott, I. Interspecific competition, island biogeography and null hypotheses. Evolution 34, 332–341 (1980).
pubmed: 28563433
doi: 10.1111/j.1558-5646.1980.tb04822.x
Thomas, C. D. Climate, climate change and range boundaries. Divers. Distrib. 16, 488–495 (2010).
doi: 10.1111/j.1472-4642.2010.00642.x
Almeida-Neto, M., Guimarães, P., Guimarães, P. R. Jr, Loyola, R. D. & Ulrich, W. A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117, 1227–1239 (2008).
doi: 10.1111/j.0030-1299.2008.16644.x
Simmons, B. I. et al. Moving from frugivory to seed dispersal: incorporating the functional outcomes of interactions in plant–frugivore networks. J. Anim. Ecol. 87, 995–1007 (2018).
pubmed: 29603211
pmcid: 6849527
doi: 10.1111/1365-2656.12831
Benadi, G., Blüthgen, N., Hovestadt, T. & Poethke, H.-J. Contrasting specialization–stability relationships in plant–animal mutualistic systems. Ecol. Model. 258, 65–73 (2013).
doi: 10.1016/j.ecolmodel.2013.03.002
Beckett, S. J. Improved community detection in weighted bipartite networks. R. Soc. Open Sci. 3, 140536 (2016).
pubmed: 26909160
pmcid: 4736915
doi: 10.1098/rsos.140536
Sonne, J. et al. Ecological mechanisms explaining interactions within plant–hummingbird networks: morphological matching increases towards lower latitudes. Proc. R. Soc. B 287, 20192873 (2020).
pubmed: 32156208
pmcid: 7126064
doi: 10.1098/rspb.2019.2873
Patefield, W. Algorithm AS 159: an efficient method of generating random R × C tables with given row and column totals. J. R. Stat. Soc. C 30, 91–97 (1981).
Dalsgaard, B. et al. Opposed latitudinal patterns of network‐derived and dietary specialization in avian plant–frugivore interaction systems. Ecography 40, 1395–1401 (2017).
doi: 10.1111/ecog.02604
Dormann, C. F., Gruber, B. & Fründ, J. Introducing the bipartite package: analysing ecological networks. R News 8, 8–11 (2008).
Holt, B. G. et al. An update of Wallace’s zoogeographic regions of the world. Science 339, 74–78 (2013).
pubmed: 23258408
doi: 10.1126/science.1228282
Two-Minute Gridded Global Relief Data (ETOPO2) v. 2 (NOAA National Geophysical Data Center, 2006); https://doi.org/10.7289/V5J1012Q
Jetz, W. & Rahbek, C. Geographic range size and determinants of avian species richness. Science 297, 1548–1551 (2002).
pubmed: 12202829
doi: 10.1126/science.1072779
Dobzhansky, T. Evolution in the tropics. Am. Sci. 38, 209–221 (1950).
Currie, D. J., Francis, A. P. & Kerr, J. T. Some general propositions about the study of spatial patterns of species richness. Écoscience 6, 392–399 (1999).
doi: 10.1080/11956860.1999.11682541
Hurlbert et al. The effect of energy and seasonality on avian species richness and community composition. Am. Nat. 161, 83–97 (2003).
pubmed: 12650464
doi: 10.1086/345459
Karger, D. N. et al. Climatologies at high resolution for the Earth’s land surface areas. Sci. Data 4, 170122 (2017).
pubmed: 28872642
pmcid: 5584396
doi: 10.1038/sdata.2017.122
Mateo, R. G., Felicísimo, Á. M. & Muñoz, J. Effects of the number of presences on reliability and stability of MARS species distribution models: the importance of regional niche variation and ecological heterogeneity. J. Veg. Sci. 21, 908–922 (2010).
doi: 10.1111/j.1654-1103.2010.01198.x
Blonder, B. et al. Linking environmental filtering and disequilibrium to biogeography with a community climate framework. Ecology 96, 972–985 (2015).
pubmed: 26230018
doi: 10.1890/14-0589.1
Vizentin-Bugoni, J., Debastiani, V. J., Bastazini, V. A. G., Maruyama, P. K. & Sperry, J. H. Including rewiring in the estimation of the robustness of mutualistic networks. Methods Ecol. Evol. 11, 106–116 (2020).
doi: 10.1111/2041-210X.13306
Rahbek, C., Borregaard, M. K., Hermansen, B., Nogues-Bravo, D. & Fjeldså, J. Definition and Description of the Montane Regions of the World (Center for Macroecology, Evolution and Climate, 2019); https://macroecology.ku.dk/resources/mountain_regions/definition-and-description-of-the-montane-regions-of-the-world_kopi/
Hothorn, T., Bretz, F. & Westfall, P. Simultaneous inference in general parametric models. Biom. J. 50, 346–363 (2008).
pubmed: 18481363
doi: 10.1002/bimj.200810425