Frugivory in canopy plants in a western Amazonian forest: Dispersal systems, phylogenetic ensembles and keystone plants

PLoS ONE

Volumn 10, Issue 10, 2015, Pages

  Stevenson, Pablo R ^a   Link, Andrés ^a   González Caro, Sebastian ^a,b   Torres Jiménez, María Fernanda ^a,c  

^a UNIVERSIDAD DE LOS ANDES   (Colombia)

^b Medellin Botanical Garden   (Colombia)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ALIBERTIA; APEIBA ASPERA; ARTICLE; BIRD; BROSIMUM ALICASTRUM; BROSIMUM GUIANENSIS; BROSIMUM LACTESCENS; BURSERA INVERSA; CANOPY; CASEARIA ACULEATA; CASTILLA ULEI; CAYAPONIA GRANATENSIS; CECROPIA ENGLERIANA; CECROPIA MEMBRANACEA; CECROPIA SCIADOPHYLLA; CELTIS SCHIPPII; CESTRUM RACEMOSUM; CLUSIA NIGROLINEATA; CLUSIA PALMICIDA; COLOMBIA; COUSSAPOA ORTHONEURA; CREPIDOSPERMUM RHOIFOLIUM; DENDROPANAX CAUCANUS; DIURNAL SPECIES; EUGENIA NESIOTICA; FICUS DAVIDSONII; FICUS INSIPIDA; FICUS SPHENOPHYLLA; FRUGIVORE; FRUGIVORY; FRUIT; GARCINIA MACROPHYLLA; GUAREA GUIDONIA; GUATTERIA; GUSTAVIA HEXAPETALA; HAPLORHINI; HELICOSTYLIS TOMENTOSA; HENRIETTELLA FISSANTHERA; HIERONYMA ALCHORNEOIDES; HYMENAEA OBLONGIFOLIA; INGA; INGA ACREANA; INGA ACROCEPHALA; INGA ALBA; INGA EDULIS; IRYANTHERA LAEVIS; JACARATIA DIGITATA; KEYSTONE SPECIES; LAETIA CORYMBULOSA; LAETIA PROCERA; LEONIA GLYCYCARPA; MAYTENUS; NECTANDRA MEMBRANACEA; NEEA; NONHUMAN; OCOTEA LONGIFOLIA; OCOTEA OBLONGA; OENOCARPUS BATAUA; OXANDRA MEDIOCRIS; PHYLOGENY; PLANT; PLANT PRODUCT; POPULATION ABUNDANCE; POPULATION DISPERSION; POUROUMA BICOLOR; POUROUMA PETIOLULATA; POUTERIA CAIMITO; POUTERIA PROCERA; PROTIUM GLABRESCENS; PROTIUM SAGOTIANUM; PSEUDOLMEDIA HIRSUTA; PSEUDOLMEDIA LAEVIGATA; PSEUDOMALMEA DICLINA; PSITTACANTHUS CUCULLARIS; RHODOSTEMONODAPHNE SYNANDRA; SAPIUM LAURIFOLIUM; SEED DISPERSAL; SOCRATEA EXORRHIZA; SOUROUBEA SYMPETALA; SPONDIAS MOMBIN; SPONDIAS VENULOSA; SWARTZIA; TALISIA INTERMEDIA; TRICHILIA PALLIDA; TRICHILIA PLEEANA; TRICHILIA TUBERCULATA; VIROLA CALOPHYLLA; VIROLA FLEXUOSA; VIROLA PERUVIANA; ANIMAL; FEEDING BEHAVIOR; FOREST; HERBIVORY; PARASITOLOGY; PHYSIOLOGY;

ANIMALS; FEEDING BEHAVIOR; FORESTS; HERBIVORY; PHYLOGENY; PLANTS; SEED DISPERSAL;

EID: 84949472145     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0140751     Document Type: Article

References (103)

1. Howe HF, Smallwood J. Ecology of seed dispersal. Annu Rev Ecol Syst. 1982; 13: 201-218.
2. Wills C, Condit R., Foster RB, Hubbell SP. Strong density- and diversity-related effects help to maintain tree species diversity in a neotropical forest. P Nat Acad Sci USA. 1997; 94: 1252-1257.
3. Wright JS. Plant diversity in tropical forests: A review of mechanisms of species coexistence. Oecologia 2002; 130: 1-14.
4. Webb CO, Peart DR. High seed dispersal rates in faunally intact tropical rain forest: Theoretical and conservation implications. Ecol Lett. 2001; 4: 491-499.
5. Swamy V, Terborgh JW. Distance-responsive natural enemies strongly influence seedling establishment patterns of multiple species in an amazonian rain forest. J Ecol. 2010; 98: 1096-1107.
6. Foster SA, Janson CH. The relationship between seed size and establishment conditions in tropical woody-plants. Ecology 1985; 66: 773-780.
7. Dalling JW, Harms KE, Aizprúa R. Seed damage tolerance and seedling resprouting ability of Prioria copaifera in Panama. J Trop Ecol. 1997; 13: 481-490.
8. Dalling JW, Harms KE. Damage tolerance and cotyledonary resource use in the tropical tree Gustavia superba. Oikos 1999; 85: 257-264.
9. Baraloto C, Forget PM. Seed size, seedling morphology, and response to deep shade and damage in neotropical rain forest trees. Am J Bot 2007; 94: 901-911. doi: 10.3732/ajb.94.6.901 PMID: 21636459
10. Ter Steege H, Pitman NCA, Phillips OL, Chave J, Sabatier D. Duque A, et al. Continental-scale patterns of canopy tree composition and function across Amazonia. Nature 2006; 443: 444-447. PMID: 17006512
11. Kidson R, Westoby M. Seed mass and seedling dimensions in relation to seedling establishment. Oecologia 2000; 125(1): 11-17.
12. Lord JM. Frugivore gape size and the evolution of fruit size and shape in southern hemisphere floras. Austral Ecol. 2004; 29: 430-436.
13. Peres CA, van Roosmalen M. Primate frugivory in two species-rich neotropical forests: Implications for the demography of large-seeded plants in overhunted areas. In: Levey DJ, Silva WR, Galetti M, editors. Seed Dispersal and Frugivory: Ecology, Evolution and Conservation. Wallingford: Cab International. 2002; pp. 407-421.
14. Tobler MW. Habitat use and diet of baird's (Tapirs tapirus bairdii) in a montane cloud forest of the Cordillera de Talamanca, Costa Rica. Biotropica 2002; 34: 468-474.
15. Stevenson PR, Pineda M, Samper T. Influence of seed size on dispersal patterns of woolly monkeys (Lagothrix lagothricha) at Tinigua Park, Colombia. Oikos 2005; 110: 435-440.
16. Jansen PA, Hirsch BT, Emsens WJ, Zamora-Gutierrez V, Wikelski M, Kays R, Thieving rodents as substitute dispersers of megafaunal seeds. P Nat Acad Sci USA. 2012; 109: 12610-12615.
17. Bollen A, van Elsacker L, Ganzhorn JU. Tree dispersal strategies in the littoral forest of Sainte Luce Se-Madagascar; Oecologia 2004; 139: 604-616. PMID: 15095087
18. Correa DF, Álvarez E, Stevenson PR. Plant dispersal systems in neotropical forests: Availability of dispersal agents or availability of resources for constructing zoochorous fruits? Global Ecol Biogeogr 2015; 24: 203-214.
19. van Roosmalen MGM. Fruits of The Guianan Flora. Wageningen: Institute of Systematic Botany Utrecht University; 1985.
20. Stevenson PR, Quiñones MJ, Castellanos MC. Guía de frutos de los bosques del Río Duda, La Macarena, Colombia. Bogotá. Asociación para la defensa de la Macarena-IUCN; 2000a.
21. Janson CH. Adaptation of fruit morphology to dispersal agents in a neotropical forest. Science 1983; 219: 187-189. PMID: 17841688
22. Snow DW. Evolutionary aspects of fruit-eating by birds. Ibis 1971; 113: 194-202.
23. Mckey D. The ecology of coevolved seed dispersal systems. In: Gilbert LE, Raven PH, editors. Coevolution of animals and plants. Austin: University of Texas Press. 1975; pp. 159-191.
24. Howe HF. Bird activity and seed dispersal of a tropical wet forest tree. Ecology 1977; 58: 539-550.
25. Howe HF. Specialized and generalized dispersal systems: Where does "the paradigm stand"? Vegetation 1993; 107/108: 3-13.
26. Böhning-Gaese K, Gaese BH, Rabemanantsoa SB. Seed dispersal by frugivorous tree visitors in malagasy tree species Commiphora guillaumini. Ecotropica 1995; 1: 41-50.
27. Fuentes M. How specialized are fruit-bird interactions? overlap of frugivore assemblages within and between plant species. Oikos 1995; 74: 324-330.
28. Larson DL. Seed dispersal by specialist versus generalist foragers: The plant's perspective. Oikos 1996; 76: 113-120.
29. Ratiarison S, Forget P. Frugivores and seed removal at Tetragastris altissima (Burseraceae) in a fragmented forested landscape of French Guiana. J Trop Ecol. 2005; 21: 501-508.
30. Schleuning M, Blüthgen N, Flörchinger JB, Schaefer M. Böhning-Gaese K. Specialization and interaction strength in a tropical plant-frugivore network differ among forest strata. Ecology 2011; 92(1): 26-36 PMID: 21560673
31. Link A, Stevenson PR. Fruit syndromes in animal dispersed plants at Tinigua Natinal Park, Colombia. Rev Chil Hist Nat. 2004; 77: 319-334.
32. Fischer KE, Chapman CA. Frugivores and fruit syndromes: Differences in patterns at the genus and species level. Oikos 1993; 66: 472-482.
33. Gautier-Hion A, Duplantier JM, Quris R, Feer F, Sourd C. Decoux JP, et al. Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia 1985; 65: 324-337.
34. Guimarães PR Jr, Galetti M, Jordano P. Seed dispersal anachronisms: Rethinking the fruits extinct megafauna ate. Plos One 2008; 3: E1745. doi: 10.1371/journal.pone.0001745 PMID: 18320062
35. Herrera CM. Correlated evolution of fruit and leaf size in bird-dispersed plants: species-level variance in fruit traits explained a bit further? Oikos 2002; 97: 426-432.
36. Schupp EW. Quantity, quality and the effectiveness of seed dispersal by animals. Vegetatio 1993; 107/108: 15-29.
37. Blüthgen N, Menzel F, Hovestadt T, Fiala B, Blüthgen N. Specialization, constraints, and conflicting interests in mutualistic networks. Curr Biol. 2007; 17: 341-346. PMID: 17275300
38. Bascompte J, Jordano P, Melián CJ, Olesen JM. The nested assembly of plant-animal mutualistic networks. Proc. Nat. Acad. Sci. USA. 2003; 100 (16): 9383-9387. PMID: 12881488
39. Webb CO, Ackerly DD, Mcpeek MA, Donoghue MJ. Phylogenies and community ecology. Annu Revi Ecol Syst. 2002; 33: 475-505.
40. Terborgh J. Keystone plant resources in the tropical forests. In: Soule ME, editor. Conservation biology: The science of scarcity and diversity. Sunderland: Sinauer. 1986; pp. 330-344.
41. Power ME, Tilman D, Estes JA, Menge BA, Bond WJ, Mills LS, et al. Challenges in the quest for keystones. Bioscience 1996; 46: 609-630.
42. Peres CA. Identifying keystone plant resources in tropical forests: the case of gums from parkia pods. J Trop Ecol. 2000; 16: 287-317.
43. Stevenson PR. Potential keystone plant species for the frugivore community at Tinigua Park, Colomba. In: Dew LJ, Boubli JP, editores. Tropical fruits and frugivores: the search for strong interactions. The Neatherlands: Springer. 2005; pp. 37-57.
44. Jordán F, Liu W, Mike A. Trophic field overlap: A new approach to quantify keystone species. Ecol Modell. 2009; 220: 2899-2907.
45. Poulsen JR, Clark CJ, Connor EF, Smith TB. Differential resource use by primates and hornbills: Implications for seed dispersal. Ecology 2002; 83: 228-240.
46. Hawes JE, Peres CA. Fruit-frugivore interactions in amazonian seasonally flooded and unflooded forests. J Trop Ecol. 2014; doi: 10.1017/S0266467414000261
47. Chapman CA, Chapman LJ. Plant-animal coevolution: Is it thwarted by spatial and temporal variation in animal foraging? In: Levey DJ, Silva WR, Galetti M, editors. Seed dispersal and frugivory: ecology, evolution and conservation. Wallingford: Cab International. 2002; pp. 275-290.
48. Herrera CM. Long-term dynamics of mediterranean frugivorous birds and fleshy fruits: A 12-year study. Ecol Monogr. 1998; 68: 511-538.
49. Sewall BJ, Freestone AL, Hawes JE, Andriamanarina E. Size-energy relationships in ecological communities. Plos One 2013; 8(8):e68657.
50. Stevenson PR, Castellanos MC, Cortes AI, Link A. Flowering patterns in a seasonal tropical lowland forest in Western Amazonia. Biotropica 2008; 40: 559-567.
51. Stevenson PR. Frugivory and seed dispersal by woolly monkeys at Tinigua National Park, Colombia. Phd. Thesis. New York: State University of New York At Stony Brook; 2002.
52. Stevenson PR, Quiñones MJ, Ahumada JA. Influence of fruit availability on ecological overlap among four neotropical primates at Tinigua National Park, Colombia. Biotropica 2000; 32: 533-544.
53. Stevenson PR. Fruit choice by woolly monkeys in Tinigua National Park, Colombia. Int J Primatol. 2004; 25: 367-381.
54. Stevenson PR. Estimates of the number of seeds dispersed by a population of primates in a lowland forest in Western Amazonia. In: Dennis AJ, Schupp EW, Green RJ, Westcott DW, editors. Seed dispersal: Theory and its application in a changing world. Wallingford: Cab International. 2007; pp. 340-362.
55. Alvarez-Rebolledo M, Mejía-Londoño GD, Umaña AM, Reyes N. Censos de aves en el Centro de Investigaciones Ecológicas La Macarena. Universidad de Los Andes. Unpublished report. 1995.
56. Webb CO, Donoghue MJ. Phylomatic: tree assembly for applied phylogenetics. Molecular Ecology Notes 2005; 5(1): 181-183
57. Wikström N, Savolainen V, Chase MW. Evolution of the angiosperms: Calibrating the family tree. P Roy Soc Lond B Bio. 2001; 268: 2211-2220.
58. Webb CO, Ackerly DD, Kembel SW. Phylocom: software for the analysis of phylogenetic community structure and trait evolution. Bioinformatics 2008; 24(18): 2098-2100. doi: 10.1093/bioinformatics/btn358 PMID: 18678590
59. Dormann CF, Gruber B, Fründ J. Introducing The Bipartite Package: Analysing ecological networks. R News 2008; 8: 8-11.
60. Martín-González AM, Dalsgaard B, Olesen JM. Centrality measures and the importance of generalist species in pollination networks. Ecol Complex. 2010; 7: 36-43.
61. Dunne JA, Williams RJ, Martinez ND. Network structure and biodiversity loss in food webs: Robustness increases with connectance. Ecol Lett. 2002; 5: 558-567.
62. Vasas V, Jordán F. Topological keystone species in ecological interaction networks: considering link quality and non-trophic effects. Ecol Model. 2006; 196: 365-378.
63. Jordán F, Liu W, Davis AJ. Topological keystone species: Measures of positional importance in food webs. Oikos 2006; 112: 535-546.
64. Jordano P, Bascompte J, Olesen JM. Invariant properties in coevolutionary networks of plant-animal interactions. Ecol Lett. 2003; 6: 69-81.
65. Bascompte J, Jordano P. Plant-animal mutualistic networks: The architecture of biodiversity. Annu Rev Ecol Evol Syst. 2007; 38: 567-593.
66. Almeida-Neto M, Guimarães P, Guimarães PR, Loyola RD, Ulrich W. A consistent metric for nestedness analysis in ecological systems: Reconciling concept and measurement. Oikos 2008; 117: 1227-1239.
67. Guimarães PJ, Guimarães P. Improving the analyses of nestedness for large sets of matrices. Environ Modell Softw. 2006; 21: 1512-1513.
68. Venables WN, Ripley BD. Modern applied statistics with S. Fourth Edition. New York: Springer; 2002.
69. Dáttilo W, Guimarães PR, Izzo TJ. Spatial structure of ant-plant mutualistic networks. Oikos 2013; 122: 1643-1648.
70. Kaiser-Bunbury CN, Muff S, Memmott J, Müller CB, Caflisch A. The robustness of pollination networks to the loss of species and interactions: A quantitative approach incorporating pollinator behaviour. Ecol Lett. 2010; 13: 442-452. doi: 10.1111/j.1461-0248.2009.01437.x PMID: 20100244
71. Dew JL. Foraging, food choice, and food processing by sympatric ripe-fruit specialists: Lagothrix lagotricha poeppigii and Ateles belzebuth belzebuth. Int J Primatol. 2005; 26: 1107-1135.
72. Chapman CA. Primate seed dispersal: Coevolution and conservation implications. Evol Anthropol. 1995; 4: 74-82.
73. Lambert JE, Garber PA. Evolutionary and ecological implications of primate seed dispersal. Am J Primatol. 1998; 45: 9-28. PMID: 9573440
74. Link A, Di Fiore A. Seed dispersal by spider monkeys and its importance in the maintenance of neotropical rain-forest diversity. J Trop Ecol. 2006; 22: 235-246.
75. Wright PC, Tecot SR, Erhart EM, Baden AL, King SJ, Grassi C. Frugivory in four sympatric lemurs: Implications for the future of Madagascar's forests. Am J Primatol. 2011; 73: 585-602. doi: 10.1002/ajp.20936 PMID: 21437928
76. Clark CJ, Poulsen JR, Parker VT. The role of arboreal seed dispersal groups on the seed rain of a lowland tropical forest 1. Biotropica 2001; 33: 606-620.
77. Donatti CI, Guimarães PR, Galetti M, Pizo MA, Marquitti FMD, Dirzo R. Analysis of a hyper-diverse seed dispersal network: modularity and underlying mechanisms: modularity in a seed dispersal network. Ecol Lett. 2011; 14: 773-781. doi: 10.1111/j.1461-0248.2011.01639.x PMID: 21699640
78. Mello MAR, Marquitti FMD, Guimarães PR, Kalko EKV, Jordano P, de Aguiar MAM. The modularity of seed dispersal: differences in structure and robustness between bat- and bird-fruit networks. Oecologia 2011; 167: 131-140. doi: 10.1007/s00442-011-1984-2 PMID: 21479592
79. Fleming TH, Kress WJ. A brief history of fruits and frugivores. Acta Ecológica 2011; 37: 521-530.
80. Peres CA, Palacios E. Basin-wide effects of game harvest on vertebrate population densities in amazonian forests: implications for animal-mediated seed dispersal. Biotropica 2007; 39: 304-315.
81. Stevenson PR, Castellanos MC, Pizarro JC, Garavito M. Effects of seed dispersal by three ateline monkey species on seed germination at Tinigua National Park, Colombia. Int J Primatol. 2002; 23: 1187-1204.
82. Fleming TH, Heithaus ER. Frugivorous bats, seed shadows, and the structure of tropical forest. Biotropica 1981; 13, 45-53.
83. Kalko EKV, Herre EA, Handley CO. Relation of fig fruit characteristics to fruit-eating bats in the New and Old World tropics. J Biogeogr. 1996; 23: 565-576.
84. Stevenson PR. The abundance of large ateline monkeys is positively associated with the diversity of plants regenerating in neotropical forests. Biotropica 2011; 43: 512-519.
85. Stevenson PR. Potential determinants of the abundance of woolly monkeys in neotropical forests. In: Defler T, Stevenson PR, editors. The woolly monkey: Behavior, ecology, conservation, systematics. New York: Springer. 2014; pp. 207-226.
86. French AR, Smith TB. Importance of body size in determining dominance hierarchies among diverse tropical frugivores. Biotropica 2005; 37: 96-101.
87. Campbell CJ, Aureli F, Chapman CA, Ramos-Fernández G, Matthews K, Russo SE, et al. Terrestrial behavior of Ateles spp. Int J Primatol. 2005; 26: 1039-1051.
88. Devictor V, Clavel J, Julliard R, Lavergne S, Mouillot D, Thuiller W, et al. Defining and measuring ecological specialization. J Appl Ecol. 2010; 47: 15-25.
89. Heindl M, Curio E. Observations of frugivorous birds at fruit-bearing plants in the North Negros Forest Reserve, Philippines. Ecotropica 1999; 5: 167-181.
90. Smith AD, Mcwilliams SR. Fruit removal rate depends on neighborhood fruit density, frugivore abundance, and spatial context. Oecologia 2014; 174: 931-942. doi: 10.1007/s00442-013-2834-1 PMID: 24305861
91. Stevenson PR. The relationship between fruit production and primate abundance in neotropical communities. Biol J Linn Soc. 2001; 72: 161-178.
92. Hanya G, Stevenson PR, van Noordwijk M, Te Wong S, Kanamori T, Kuze N, et al. Seasonality in fruit availability affects frugivorous primate biomass and species richness. Ecography 2011; 34: 1009-1017.
93. Nunez-Iturri G, Howe HF. Bushmeat and the fate of trees with seeds dispersed by large primates in a lowland rain forest in Western Amazonia. Biotropica 2007; 39: 348-354.
94. Terborgh J, Nuñez-Iturri G, Pitman NCA, Valverde FHC, Alvarez P, Swamy V, et al. Tree recruitment in an empty forest. Ecology 2008; 89: 1757-1768. PMID: 18589539
95. Wright DH. A simple, stable model of mutualism incorporating handling time. Am Nat. 1989; 134: 664-667.
96. Yu DW. Parasites of mutualisms. Biol J Linn Soc. 2001; 72: 529-546.
97. Alarcon R, Waser NM, Ollerton J. Year-to-year variation in the topology of a plantpollinator interaction network. Oikos 2008; 117: 1796-1807.
98. Dormann CF. How to be a specialist? Quantifying specialisation in pollination networks. Netw Biol. 2011; 1: 1-20.
99. Barrat A, Barthelemy M, Pastor-Satorras R, Vespignani A. The architecture of complex weighted networks. P Nat Acad Sci USA. 2004; 101: 3747-3752.
100. Bascompte J, Jordano P, Olesen JM. Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 2006; 312: 431-433. PMID: 16627742
101. Bersier LF, Banasšek-Richter C, Cattin MF. quantitative descriptors of food-web matrices. Ecology 2002; 83: 2394-2407.
102. Julliard R, Clavel J, Devictor V, Jiguet F, Couvet D. Spatial segregation of specialists and generalists in bird communities. Ecol Lett. 2006; 9: 1237-1244. PMID: 17040326
103. Blüthgen N, Menzel F, Blüthgen N. Measuring specialization in species interaction networks. Bmc Ecology 2006; 6: 9-9. PMID: 16907983