Oilbirds disperse large seeds at longer distance than extinct megafauna

Terborgh, J. et al. Tree recruitment in an empty forest. J. Ecol. 89, 1757–1768 (2008).

Article  Google Scholar 

Stevenson, P. The abundance of large ateline monkeys is positively associated with the diversity of plants regenerating in Neotropical forests. Biotropica 43, 512–519 (2011).

Article  Google Scholar 

Peres, C., Emilio, T., Schietti, J., Desmoulière, S. & Levi, T. Dispersal limitation induces long-term biomass collapse in overhunted Amazonian forests. Proc. Natl. Acad. Sci. 113, 892–897 (2016).

CAS  PubMed  Article  ADS  Google Scholar 

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

PubMed  PubMed Central  Article  ADS  CAS  Google Scholar 

Chanthorn, W., Hartig, F., Brockelman, W. Y., Srisang, W., Nathalang, A. & Santon, J. Defaunation of large-bodied frugivores reduces carbon storage in a tropical forest of Southeast Asia. Sci. Rep. 9 (2019).

Davis, M. & Shaw, R. Range shifts and adaptive responses to quaternary climate change. Science 292, 673–679 (2001).

CAS  PubMed  Article  ADS  Google Scholar 

Corlett, R. T. Seed dispersal distances and plant migration potential in tropical East Asia. Biotropica 41, 592–598 (2009).

Article  Google Scholar 

Duque, A., Stevenson, P. & Feeley, K. Thermophilization of adult and juvenile tree communities in the northern tropical Andes. Proc. Natl. Acad. Sci. 112, 10744–10749 (2015).

CAS  PubMed  Article  ADS  Google Scholar 

Howe, H. & Smallwood, J. Ecology of seed dispersal. Annu. Rev. Ecol. Syst. 13, 201–228 (1982).

Article  Google Scholar 

Wright, S. J. Plant diversity in tropical forests: A review of mechanisms of species coexistence. Oecologia 130, 1–14 (2002).

PubMed  Article  ADS  Google Scholar 

Sugiyama, A., Comita, L., Masaki, T., Condit, R. & Hubbell, S. Resolving the paradox of clumped seed dispersal: Positive density and distance dependence in a bat-dispersed species. Ecology 99, 2583–2591 (2018).

PubMed  Article  Google Scholar 

Bagchi, R. et al. Spatial patterns reveal negative density dependence and habitat associations in tropical trees. Ecology 92, 1723–1729 (2011).

PubMed  Article  Google Scholar 

Clark, J.S. Why trees migrate so fast: Confronting theory with dispersal biology and the paleorecord. Am. Nat. 152, 204-224 (1998)

Nathan, R. Long-distance dispersal of plants. Science 313, 786–788 (2006).

CAS  PubMed  Article  ADS  Google Scholar 

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

PubMed  Article  Google Scholar 

Abedi-Lartey, M., Dechmann, D. K. N., Wikelski, M., Scharf, A. K. & Fahr, J. Long-distance seed dispersal by straw-coloured fruit bats varies by season and landscape. Glob. Ecol. Conserv. 7, 12–24 (2016).

Article  Google Scholar 

Baraloto, C., Forget, P. M. & Goldberg, D. E. Seed mass, seedling size and Neotropical tree seedling establishment. J. Ecol. 96, 1156–1166 (2005).

Article  CAS  Google Scholar 

Mack, A. L. An advantage of large seed size: tolerating rather than succumbing to seed predators. Biotropica 30, 604–608 (1998).

Article  Google Scholar 

Peres, C. A., Roosmalen, M. V., Levey, D. J., Silva, W. & Galetti, M. Primate frugivory in two species-rich Neotropical forests: implications for the demography of large-seeded plants in overhunted areas. In Seed dispersal and frugivory: ecology, evolution and conservation (eds. Levey Silva, D. J. W. & Galetti, M.) 407–421 (Wallingford: CAB International, 2002).

Galetti, M. & Dirzo, R. Ecological and evolutionary consequences of living in a defaunated world. Biol. Conserv. 163, 1–6 (2013).

Article  Google Scholar 

Doughty, C., Wolf, A. & Malhi, Y. The legacy of the Pleistocene megafauna extinctions on nutrient availability in Amazonia. Nat. Geosci. 6, 761–764 (2013).

CAS  Article  ADS  Google Scholar 

Galetti, M. et al. Ecological and evolutionary legacy of megafauna extinctions. Biol. Rev. Camb. Philos. Soc. 93, 845–862 (2018).

PubMed  Article  Google Scholar 

Pires, M., Guimarães, P., Galetti, M. & Jordano, P. Pleistocene megafaunal extinctions and the functional loss of long-distance seed-dispersal services. Ecography 41, 153–163 (2017).

Article  Google Scholar 

Bosque, C. & Parra, O. Digestive efficiency and rate of food passage in oilbird nestlings. The Condor 94, 557–571 (1992).

Article  Google Scholar 

Rojas-Lizarazo, G. Diet and reproduction in a high mountain oilbird (Steatornis caripensis) colony in Colombia. Ornitol. Colomb. 53–69 (2016).

Stevenson, P., Cardona, L., Acosta Rojas, D., Henao Díaz, F. & Cardenas, S. Diet of oilbirds (Steatornis caripensis) in Cueva de los Guácharos National Park (Colombia): Temporal variation in fruit consumption, dispersal and seed morphology. Ornitol. Neotrop. 28, 295–307 (2017).

Google Scholar 

McAtee, W. L. Notes on the food of the Guacharo (Steatornis caripensis). Auk 39, 108–109 (1922).

Article  Google Scholar 

Holland, R. A., Wikelski, M., Kümmeth, F. & Bosque, C. The secret life of oilbirds: New insights into the movement ecology of a unique avian frugivore. PLoS ONE 4, e8264 (2009).

PubMed  PubMed Central  Article  ADS  CAS  Google Scholar 

Karubian, J. et al. Seed dispersal by Neotropical birds: Emerging patterns and underlying processes. Ornitol. Neotrop. 23, 9–24 (2012).

Google Scholar 

McKey, D. In Coevolution of animals and plants (eds. Gilben, L. E. & Raven, P. H.) 159–191 (University Texas Press, 1975).

Cárdenas, S., Cardona, L. M., Echeverry-Galvis, M. & Stevenson, P. R. Movement patterns and habitat preference of oilbirds (Steatornis caripensis) in the southern Andes of Colombia. Avian Cons. Ecol. 15, 5 (2020).

Google Scholar 

Cárdenas, S., Echeverry-Galvis, M. & Stevenson, P. R. Seed dispersal effectiveness by oilbirds (Steatornis caripensis) in the Southern Andes of Colombia. Biotropica. https://doi.org/10.1111/btp.12908 (2020).

Article  Google Scholar 

Anderson, J. T., Nuttle, T., Saldaña Rojas, J. S., Pendergast, T. H. & Flecker, A. S. Extremely long-distance seed dispersal by an overfished Amazonian frugivore. Proc. R. Soc. Lond., Ser. B: Biol. Sci. 278, 3329–3335 (2011).

Google Scholar 

Wood, C. A. The Polynesian fruit pigeon, Globicera pacifica, its food and digestive apparatus. Auk 41, 433–438 (1924).

Article  Google Scholar 

Stocker, G. C. & Irvine, A. K. Seed dispersal by cassowaries (Casuarius casuarius) in North Queensland’s Rainforests. Biotropica 15, 170–176 (1983).

Article  Google Scholar 

Gautier-Hion, A. et al. Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 65, 324–337 (1985).

CAS  PubMed  Article  ADS  Google Scholar 

Lieberman, D., Lieberman, M. & Martin, C. Notes on seeds in elephant dung from Bia National Park Ghana. Biotropica 19, 365 (1987).

Article  Google Scholar 

Guillotin, M., Dubost, G. & Sabatier, D. Food choice and food competition among the three major primate species of French Guiana. J. Zool. 233, 551–579 (1994).

Article  Google Scholar 

Fragoso, J. M. V. & Huffman, J. M. Seed-dispersal and seedling recruitment patterns by the last Neotropical megafaunal element in Amazonia, the tapir. J. Trop. Ecol. 16, 369–385 (2000).

Article  Google Scholar 

Naranjo, E. Ecology and conservation of Baird’s Tapir in Mexico. Trop. Conserv. Sci. 2, 140–158 (2009).

Article  Google Scholar 

Kitamura, S., Madsri, S. & Poonswad, P. Characteristics of hornbill-dispersed fruits in lowland Dipterocarp forests of southern Thailand. Raffles Bul. Zool. 24, 137–147 (2011).

Google Scholar 

Stevenson, P., Link, A., Onshuus, A., Quiroz, A. & Velasco, M. Estimation of seed shadows generated by Andean woolly monkeys (Lagothrix lagothricha lugens). Int. J. Primatol. 35, 1021–1036 (2014).

Article  Google Scholar 

Chen, S. C. & Moles, A. T. A mammoth mouthful? A test of the idea that larger animals ingest larger seeds. Global Ecol. Biogeogr. 24, 1269–1280 (2015).

Article  Google Scholar 

Norconk, M., Grafton, B. & Conklin-Brittain, N. Seed dispersal by Neotropical seed predators. Am. J. Primatol. 45, 103–126 (1998).

CAS  PubMed  Article  Google Scholar 

Lord, J. M. Frugivore gape size and the evolution of fruit size and shape in southern hemisphere floras. Austral Ecol. 29, 430–436 (2004).

Article  Google Scholar 

Vellend, M., Myers, J., Gardescu, S. & Marks, P. Dispersal of Trillium seeds by deer: Implications for long-distance migration of forest herbs. Ecology 84, 1067–1072 (2003).

Article  Google Scholar 

Baños-Villalba, A. et al. Seed dispersal by macaws shapes the landscape of an Amazonian ecosystem. Sci. Rep. 7 (2017).

PubMed  PubMed Central  Article  ADS  CAS  Google Scholar 

Jansen, P. et al. Thieving rodent as substitute dispersers of megafaunal seeds. Proc. Natl. Acad. Sci. 109, 12610–12615 (2012).

CAS  PubMed  Article  ADS  Google Scholar 

Blanco, G., Tella, J. L., Hiraldo, F. & Díaz-Luque, J. A. Multiple external seed dispersers challenge the megafaunal syndrome anachronism and the surrogate ecological function of livestock. Front. Ecol. Evol. 7, 328 (2019).

Article  Google Scholar 

Prada, C. & Stevenson, P. Plant composition associated with environmental gradients in tropical montane forests (Cueva de Los Guácharos National Park, Huila, Colombia). Biotropica 48, 568–576 (2016).

Article  Google Scholar 

Bosque, C. & Parra, O. Digestive efficiency and rate of food passage in oilbird nestlings. The Condor 94, 557–571 (1992).

Article  Google Scholar 

Calenge, C. The package “adehabitat” for the R software: A tool for the analysis of space and habitat use by animals. Ecol. Model. 197, 516–519 (2006).

Article  Google Scholar 

R Core Team. R: A language and environment for statistical computing. (R Foundation for Statistical Computing, Vienna, Austria 2014).

Chen, S. C. & Moles, A. T. A mammoth mouthful? A test of the idea that larger animals ingest larger seeds. Glob. Ecol. Biogeogr. 24, 1269–1280 (2015).

Article  Google Scholar 

Fox, J. & Weisberg, S. An R Companion to Applied Regression, Third edition. Sage, Thousand Oaks CA https://socialsciences.mcmaster.ca/jfox/Books/Companion/ (2019).