Downsizing of animal communities triggers stronger functional than structural decay in seed-dispersal networks

Dirzo, R. et al. Defaunation in the anthropocene. Science 345, 401–406 (2014).

McCauley, D. J. et al. Marine defaunation: animal loss in the global ocean. Science 347, 1255641–1255641 (2015).

Brose, U. et al. Predicting the consequences of species loss using size-structured biodiversity approaches. Biol. Rev. 92, 684–697 (2016).

Heinen, J. H., Van Loon, E. E., Hansen, D. M. & Kissling, W. D. Extinction-driven changes in frugivore communities on oceanic islands. Ecography 41, 1245–1255 (2017).

Kurten, E. L. Cascading effects of contemporaneous defaunation on tropical forest communities. Biol. Conserv. 163, 22–32 (2013).

Schulze, K. et al. An assessment of threats to terrestrial protected areas. Conserv. Lett. 11, e12435–11 (2018).

Pérez-Méndez, N., Jordano, P., García, C. & Valido, A. The signatures of anthropocene defaunation: cascading effects of the seed dispersal collapse. Sci. Rep. 6, 1–9 (2016).

Young, H. S., McCauley, D. J., Galetti, M. & Dirzo, R. Patterns, causes, and consequences of anthropocene defaunation. Annu. Rev. Ecol. Evol. Syst. 47, 333–358 (2016).

Cardinale, B. J. et al. Biodiversity loss and its impact on humanity. Nature 486, 59–67 (2012).

Truchy, A., Angeler, D. G., Sponseller, R. A., Johnson, R. K. & McKie, B. G. Linking biodiversity, ecosystem functioning and services, and ecological resilience: towards an integrative framework for improved management. Adv. Ecol. Res. 53, 55–96 (2015). Academic Press.

Schleuning, M., Fründ, J. & García, D. Predicting ecosystem functions from biodiversity and mutualistic networks: an extension of trait-based concepts to plant-animal interactions. Ecography 38, 380–392 (2015).

Bellwood, D. R., Streit, R. P., Brandl, S. J. & Tebbett, S. B. The meaning of the term ‘function’ in ecology: a coral reef perspective. Funct. Ecol. 33, 948–961 (2019).

Larsen, T. H., Williams, N. M. & Kremen, C. Extinction order and altered community structure rapidly disrupt ecosystem functioning. Ecol. Lett. 8, 538–547 (2005).

Lavorel, S. & Garnier, E. Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Funct. Ecol. 16, 545–556 (2002).

Heilpern, S. A., Weeks, B. C. & Naeem, S. Predicting ecosystem vulnerability to biodiversity loss from community composition. Ecology 99, 1099–1107 (2018).

Bascompte, J. & Jordano, P. Mutualistic Networks. 70 (Princeton University Press, New Jersey, 2014).

Schleuning, M. et al. Ecological networks are more sensitive to plant than to animal extinction under climate change. Nat. Commun. 7, 13965 (2016).

Dehling, D. M., Jordano, P., Schaefer, H. M., Böhning Gaese, K. & Schleuning, M. Morphology predicts species’ functional roles and their degree of specialization in plant–frugivore interactions. Proc. R. Soc. B 283, 20152444 (2016).

Bender, I. M. A. et al. Morphological trait matching shapes plant–frugivore networks across the Andes. Ecography 41, 1910–1919 (2018).

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).

Donoso, I., Schleuning, M., García, D. & Fründ, J. Defaunation effects on plant recruitment depend on size matching and size trade-offs in seed-dispersal networks. Proc. R. Soc. B 284, 20162664 (2017).

Pérez-Méndez, N., Jordano, P. & Valido, A. Persisting in defaunated landscapes: reduced plant population connectivity after seed dispersal collapse. J. Ecol. 106, 936–947 (2017).

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).

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).

Naniwadekar, R., Chaplod, S., Datta, A., Rathore, A. & Sridhar, H. Large frugivores matter: Insights from network and seed dispersal effectiveness approaches. J. Anim. Ecol. 88, 1250–1262 (2019).

Valiente-Banuet, A. et al. Beyond species loss: the extinction of ecological interactions in a changing world. Funct. Ecol. 29, 299–307 (2014).

Bello, C. et al. Defaunation affects carbon storage in tropical forests. Sci. Adv. 1, e1501105 (2015).

Osuri, A. M. et al. Contrasting effects of defaunation on aboveground carbon storage across the global tropics. Nat. Commun. 7, 11351 (2016).

Wenny, D. G., Sekercioglu, C. H., Cordeiro, N. J., Rogers, H. S. & Kelly, D. Seed Dispersal by Fruit-Eating Birds in Why Birds Matter: Avian Ecological Function and Ecosystem Services. (The University of Chicago Press, London, 2016).

Bagchi, R. et al. Defaunation increases the spatial clustering of lowland Western Amazonian tree communities. J. Ecol. 106, 1470–1482 (2018).

Nathan, R. et al. Mechanisms of long-distance seed dispersal. Trends Ecol. Evol. 23, 638–647 (2008).

García, C. & Borda-de-Água, L. Extended dispersal kernels in a changing world: insights from statistics of extremes. J. Ecol. 105, 63–74 (2016).

Schleuning, M. et al. Trait-based assessments of climate-change impacts on interacting species. Trends Ecol. Evol. 35, 319–328 (2020).

Jordano, P., Garcia, C., Godoy, J. A. & Garcia-Castano, J. L. Differential contribution of frugivores to complex seed dispersal patterns. Proc. Natl Acad. Sci. USA 104, 3278–3282 (2007).

Morales, J. M., García, D., Martínez, D., Rodriguez-Pérez, J. & Herrera, J. M. Frugivore behavioural details matter for seed dispersal: a multi-species model for cantabrian thrushes and trees. PLoS ONE 8, e65216–12 (2013).

Rehm, E., Fricke, E., Bender, J., Savidge, J. & Rogers, H. Animal movement drives variation in seed dispersal distance in a plant–animal network. Proc. R. Soc. B 286, 20182007 (2019).

Sorensen, M. C., Schleuning, M., Donoso, I., Neuschulz, E. L. & Mueller, T. Community-wide seed dispersal distances peak at low levels of specialisation in size-structured networks. Preprint at https://doi.org/10.1101/2020.02.23.958454 (2020).

Spiegel, O. & Nathan, R. Incorporating dispersal distance into the disperser effectiveness framework: frugivorous birds provide complementary dispersal to plants in a patchy environment. Ecol. Lett. 10, 718–728 (2007).

García, D., Donoso, I. & Rodriguez-Pérez, J. Frugivore biodiversity and complementarity in interaction networks enhance landscape‐scale seed dispersal function. Funct. Ecol. 32, 2742–2752 (2018).

Blüthgen, N. & Klein, A. M. Functional complementarity and specialisation: the role of biodiversity in plant-pollinator interactions. Basic Appl. Ecol. 12, 282–291 (2011).

Peralta, G., Frost, C. M., Rand, T. A., Didham, R. K. & Tylianakis, J. M. Complementarity and redundancy of interactions enhance attack rates and spatial stability in host–parasitoid food webs. Ecology 95, 1888–1896 (2014).

Poisot, T., Mouquet, N. & Gravel, D. Trophic complementarity drives the biodiversity-ecosystem functioning relationship in food webs. Ecol. Lett. 16, 853–861 (2013).

Muñoz, M. C., Schaefer, H. M., Böhning Gaese, K. & Schleuning, M. Importance of animal and plant traits for fruit removal and seedling recruitment in a tropical forest. Oikos 126, 823–832 (2016).

Dugger, P. J. et al. Seed-dispersal networks are more specialized in the Neotropics than in the Afrotropics. Glob. Ecol. Biogeogr. 28, 248–261 (2019).

Morais-Vidal, M. et al. Predicting the non‐linear collapse of plant–frugivore networks due to habitat loss. Ecography 42, 1765–1776 (2019).

Brodie, J. F. et al. Secondary extinctions of biodiversity. Trends Ecol. Evol. 29, 664–672 (2014).

Galetti, M. et al. Ecological and evolutionary legacy of megafauna extinctions. Biol. Rev. 93, 845–862 (2017).

Schleuning, M. et al. Specialization of mutualistic interaction networks decreases toward tropical latitudes. Curr. Bio. 22, 1925–1931 (2012).

Bender, I. M. A. et al. Functionally specialised birds respond flexibly to seasonal changes in fruit availability. J. Anim. Ecol. 86, 800–811 (2017).

Kelly, E. L. A. et al. Investigating functional redundancy versus complementarity in Hawaiian herbivorous coral reef fishes. Oecologia 182, 1151–1163 (2016).

Timóteo, S., Ramos, J. A., Vaughan, I. P. & Memmott, J. High resilience of seed dispersal webs highlighted by the experimental removal of the dominant disperser. Curr. Biol. 26, 910–915 (2016).

Tylianakis, J. M. & Morris, R. J. Ecological networks across environmental gradients. Annu. Rev. Ecol. Evol. Syst. 48, 25–48 (2017).

Eskildsen, A. et al. Ecological specialization matters: long-term trends in butterfly species richness and assemblage composition depend on multiple functional traits. Divers. Distrib. 21, 792–802 (2015).

Stork, N. E. et al. Vulnerability and resilience of tropical forest species to land-use change. Conserv. Biol. 23, 1438–1447 (2009).

Pearson, R. G. et al. Life history and spatial traits predict extinction risk due to climate change. Nat. Clim. Change 4, 217–221 (2014).

Yachi, S. & Loreau, M. Biodiversity and ecosystem productivity in a fluctuating environment: The insurance hypothesis. Proc. Natl Acad. Sci. USA 96, 1463–1468 (1999).

Fricke, E. C., Tewksbury, J. J. & Rogers, H. S. Defaunation leads to interaction deficits, not interaction compensation, in an island seed dispersal network. Glob. Change Biol. 24, e190–e200 (2017).

Marjakangas, E. L. et al. Fragmented tropical forests lose mutualistic plant–animal interactions. Divers. Distrib. 17, 503–515 (2019).

Ovaskainen, O. et al. Joint species movement modeling: how do traits influence movements? Ecology 100, e02622 (2019).

Morán López, T. et al. Can network metrics predict vulnerability and species roles in bird‐dispersed plant communities? Not without behaviour. Ecol. Lett. 8, 8–11 (2019).

Terborgh, J. The big things that run the world - a sequel to E. O. Wilson. Conserv. Biol. 2, 402–403 (1988).

Dirzo, R. & Miranda, A. Contemporary neotropical defaunation and forest structure, function, and diversity - a sequel to John Terborgh. Conserv. Biol. 4, 444–447 (1990).

Bender, I. M. A. et al. Morphological trait matching shapes plant–frugivore networks across the Andes [Dataset]. Ecography https://doi.org/10.12761/SGN.2018.10237 (2018).

Wilman, H. et al. EltonTraits 1.0: species-level foraging attributes of the world’s birds and mammals. Ecology 95, 2027 (2014).

Pires, M. M., Guimarães, P. R., Galetti, M. & Jordano, P. Pleistocene megafaunal extinctions and the functional loss of long-distance seed-dispersal services. Ecography 41, 153–163 (2018).

Donoso, I., García, D., Rodriguez-Pérez, J. & Martínez, D. Incorporating seed fate into plant-frugivore networks increases interaction diversity across plant regeneration stages. Oikos 125, 1762–1771 (2016).

Robbins, C. T. Food Intake Regulation in Wildlife Feeding and Nutrition. (Academic Press, London, 1983).

Levey, D. J. Methods of seed processing by birds and seed deposition patterns. In Frugivoresand Seed Dispersal 147–158 (Springer, Dordrecht, 1986).

Uriarte, M. et al. Disentangling the drivers of reduced long-distance seed dispersal by birds in an experimentally fragmented landscape. Ecology 92, 924–937 (2011).

Gasperin, G. & Pizo, M. A. Passage time of seeds through the guts of frugivorous birds, a first assessment in Brazil. Rev. Bras. Ornitol. 20, 48–51 (2012).

Schurr, F. M. Long-distance seed dispersal. Ann. Plant Rev. 38, 204–237 (2009).

Viana, D. S., Santamaría, L., Michot, T. C. & Figuerola, J. Allometric scaling of long-distance seed dispersal by migratory birds. Am. Nat. 181, 649–662 (2013).

Tucker, V. A. Energetics of Natural Avian Flight in Avian Energetics. pp. 298–333. (Nuttal Ornithological Club, Cambridge, MA, USA, 1974).

Guttal, V., Bartumeus, F., Hartvigsen, G. & Nevai, A. L. Retention time variability as a mechanism for animal mediated long-distance dispersal. PLoS ONE 6, e28447–10 (2011).

Bruderer, B. & Boldt, A. Flight characteristics of birds: I. Radar measurements of speeds. Ibis 143, 178–204 (2001).

Alerstam, T., Rosén, M., Bäckman, J., Ericson, P. G. P. & Hellgren, O. Flight speeds among bird species: allometric and phylogenetic effects. PLoS Biol. 5, e197 (2007).

R Core Team, R. A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, Vienna, Austria, 2017).