Skip to main content Accessibility help

How do fruit productivity, fruit traits and dietary specialization affect the role of birds in a mutualistic network?

  • Marcia L. Malanotte (a1), Tiago Machado-de-Souza (a1), Ricardo P. Campos (a1), Carmen L.O. Petkowicz (a2) and Isabela G. Varassin (a3)...


Many plant traits might explain the different ecological and network roles of fruit-eating birds. We assessed the relationship of plant productivity, fruit traits (colour, seed size and nutritional quality) and dietary specialization, with the network roles of fruit-eating birds (number of partners, centrality and selectivity) in the Atlantic Forest, Brazil. We classified bird species according to their dietary specialization into three categories: obligate, partial and opportunistic fruit-eating birds. To test if network roles changed according to dietary specialization, fruit productivity and traits, we used a generalized linear model analysis. The selected 14 species of plant interacted with 52 bird species, which consumed 2199 fruits. The most central and generalist fruit-eating bird, Turdus albicolis, interacted with plants that produced more fruits, such as Miconia cinerascens, and had, on average, larger seeds, such as Myrcia splendens. The most selective birds interacted with fruits with a higher concentration of lipids and less intense colour, and plants that produced fewer fruits. Obligate fruit-eating birds, such as Patagioenas plumbea, were more selective than partial and opportunistic birds. Different plant traits are therefore related to the different network roles of fruit-eating birds in the Atlantic Forest, which are also dependent on bird dietary specialization.


Corresponding author

*Author for correspondence: Marcia L. Malanotte, Email:


Hide All
AOAC (1990) Official Methods of Analysis of AOAC International (15th edition). Washington, DC: AOAC International, 684 pp.
Bascompte, J and Jordano, P (2007) The structure of plant–animal mutualistic networks. In Pascual, M and Dunne, J (eds), Ecological Networks. Oxford: Oxford University Press, pp. 143159.
Bender, IM, Kissling, WD, Blendinger, PG, Böhning-Gaese, K, Hensen, I, Kühn, I, Muñoz, MC, Neuschulz, EL, Nowak, L, Quitián, M, Saavedra, F, Santillán, V, Töpfer, T, Wiegand, T, Dehling, M and Schleuning, M (2018) Morphological trait matching shapes plant–frugivore networks across the Andes. Ecography 41, 19101919.
Blendinger, PG, Giannini, NP, Zampini, IC, Ordoñez, R, Torres, S, Sayago, JE, Ruggera, RA and Isla, MI (2015) Nutrients in fruits as determinants of resource tracking by birds. Ibis 157, 480495.
Blendinger, PG, Martín, E, Acosta, OO, Ruggera, RA and Aráoz, E (2016) Fruit selection by Andean forest birds: influence of fruit functional traits and their temporal variation. Biotropica 48, 677686.
Blüthgen, N, Menzel, F and Blüthgen, N (2006) Measuring specialization in species interaction networks. BioMed Central Ecology 6, 9.
Burns, KC (2006) A simple null model predicts fruit–frugivore interactions in a temperate rainforest. Oikos 115, 427432.
Burns, KC (2013) What causes size coupling in fruit–frugivore interaction webs? Ecology 94, 295300.
Burns, JH and Strauss, SY (2011) More closely related species are more ecologically similar in an experimental test. Proceedings of the National Academy of Sciences USA 108, 53025307.
Cárdenas-Pérez, S, Chanona-Pérez, J, Méndez-Méndez, JV, Calderón-Domínguez, G, López-Santiago, R, Perea-Flores, MJ and Arzate-Vázquez, I (2017) Evaluation of the ripening stages of apple (Golden Delicious) by means of computer vision system. Biosystems Engineering 159, 4658.
Carlo, TA, Collazo, JA and Groom, MJ (2003) Avian fruit preferences across a Puerto Rican forested landscape: pattern consistency and implications for seed removal. Oecologia 134, 119131.
Cazetta, E, Schaefer, HM and Galetti, M (2009) Why are fruits colorful? The relative importance of achromatic and chromatic contrasts for detection by birds. Evolutionary Ecology 23, 233244.
Cazetta, E, Galetti, M, Rezende, EL and Schaefer, HM (2012) On the reliability of visual communication in vertebrate-dispersed fruits. Journal of Ecology 100, 277286.
Chaplin, MF and Kennedy, JF (1994) Carbohydrate Analysis: A Practical Approach. Oxford: Oxford University Press, 324 pp.
Chapman, CA, Chapman, LJ, Wangham, R, Hunt, K, Gebo, D and Gardner, L (1992) Estimators of fruit abundance of tropical trees. Biotropica 24, 527531.
Crampton, LH, Longland, WS, Murphy, DD and Sedinger, JS (2011) Food abundance determines distribution and density of a frugivorous bird across seasons. Oikos 120, 6576.
Dehling, DM, Töpfer, T, Schaefer, M, Jordano, P, Böhning-Gaese, K and Schleuning, M (2014) Functional relationships beyond species richness patterns: trait matching in plant–bird mutualisms across scales. Global Ecology Biogeography 23, 10851093.
Dormann, CF (2011) How to be a specialist? Quantifying specialisation in pollination networks. Network Biology 1, 120.
Eklöf, A, Jacob, U, Kopp, J, Bosch, J, Castro-Urgal, R, Chacoff, NP, Dalsgaard, B, Sassi, C, Galetti, M, Guimarães, PR, Lomáscolo, SB, Martín González, AM, Pizo, MA, Rader, R, Rodrigo, A, Tylianakis, JM, Vázquez, DP and Allesina, S (2013) The dimensionality of ecological networks. Ecology Letters 16, 577583.
Endler, JA (1990) On the measurement and classification of color in studies of animal color patterns. Biological Journal of the Linnean Society 41, 315352.
Fleming, TH (1979) Do tropical frugivores compete for food? American Zoologist 19, 11571172.
Fleming, TH, Venable, DL and Herrera, LGM (1993) Opportunism vs. specialization: the evolution of dispersal strategies in fleshy-fruited plants. Vegetatio 108, 107120.
Galetti, M, Pizo, MA and Morellato, LPC (2011) Diversity of functional traits of fleshy fruits in a species-rich Atlantic rain forest. Biota Neotropica 11, 181193.
Gleditsch, JM and Carlo, TA (2011) Fruit quantity of invasive shrubs predicts the abundance of common native avian frugivores in central Pennsylvania. Diversity and Distributions 17, 244253.
González-Castro, A, Yang, S, Nogales, M and Carlo, TA (2015) Relative importance of phenotypic trait matching and species’ abundances in determining plant–avian seed dispersal interactions in a small insular community. AoB Plants 7, 110.
Guida, V, Ferrari, G, Pataro, G, Chambery, A, Di Maro, A and Parente, A (2013) The effects of ohmic and conventional blanching on the nutritional, bioactive compounds and quality parameters of artichoke heads. LWT–Food Science and Technology 53, 569579.
Howe, HF (1986) Seed dispersal by fruit-eating birds and mammals. In Murray, DR (ed.), Seed Dispersal. New York, NY: Academic Press, pp. 123189.
Howe, HF (1993) Specialized and generalized dispersal systems: where does ‘the paradigm’ stand? Vegetatio 107, 313.
Hoyo, JD, Elliott, A and Christie, D (2010) Handbook of the Birds of the World (Vol. 15). Barcelona: Lynx Ediciones, 879 pp.
Jordano, P (1987) Frugivory, external morphology and digestive system in Mediterranean sylviid warblers Sylvia spp. Ibis 129, 175189.
Jordano, P (1995) Frugivore-mediated selection on fruit and seed size: birds and St. Lucie’s cherry, Prunus mahaleb. Ecology 76, 26272639.
Jordano, P (2000) Fruits and frugivory. In Fenner, M (ed.), Seeds: The Ecology of Regeneration in Natural Plant Communities. Wallingford: CAB International, pp. 125166.
Jordano, P, Forget, PM, Lambert, JE, Böhning-Gaese, K, Traveset, A and Wright, SJ (2011) Frugivores and seed dispersal: mechanisms and consequences for biodiversity of a key ecological interaction. Biology Letters 7, 321323.
Kauano, EE, Torezan, JMD, Cardoso, FCG and Marques, MCM (2012) Landscape structure in the northern coast of Paraná state, a hotspot for the Brazilian Atlantic Forest conservation. Revista Árvore 36, 961970.
Kissling, WD, Rahbek, C and Böhning-Gaese, K (2007) Food plant diversity as broad-scale determinant of avian frugivore richness. Proceedings of the Royal Society of Edinburgh Section B, Biological Sciences 274, 799808.
Kissling, WD, Böhning-Gaese, K and Jetz, W (2009) The global distribution of frugivory in birds. Global Ecology and Biogeography 18, 150162.
Landherr, A, Friedl, B and Heidemann, J (2010) A critical review of centrality measures in social networks. Business & Information Systems Engineering 2, 371385.
Levey, DJ (1988) Spatial and temporal variation in Costa Rican fruit and fruit-eating bird abundance. Ecological Monographs 58, 251269.
Loiselle, BA and Blake, JG (1990) Diets of understory fruit-eating birds in Costa Rica: seasonality and resource abundance. Studies in Avian Biology 13, 91103.
Mack, AL (1990) Is frugivory limited by secondary compounds in fruits? Oikos 57, 135138.
Machado-de-Souza, T, Campos, RP, Devoto, M and Varassin, IG (2019) Local drivers of the structure of a tropical bird-seed dispersal network. Oecologia 189, 113.
Martín González, AM, Dalsgaard, B and Olesen, JM (2010) Centrality measures and the importance of generalist species in pollination networks. Ecological Complexity 7, 3643.
McKey, D (1975) The ecology of coevolved seed dispersal systems. In Gilbert, LE and Raven, PH (eds), Coevolution of Animals and Plants. Austin, TX: University of Texas Press, pp. 159191.
Mello, MAR, Rodrigues, FA, Costa, LDF, Kissling, WD, Sekercioğlu, ÇH, Marquitti, FMD and Kalko, EKV (2015) Keystone species in seed dispersal networks are mainly determined by dietary specialization. Oikos 124, 10311039.
Memmott, J, Waser, NM and Price, MV (2004) Tolerance of pollination networks to species extinctions. Proceedings of the Royal Society B, Biological Sciences 271, 26052611.
Moegenburg, SM and Levey, DJ (2003) Do frugivores respond to fruit harvest? An experimental study of short-term responses. Ecology 84, 26002612.
Moermond, TC and Denslow, JS (1985) Neotropical avian frugivores: patterns of behavior, morphology, and nutrition, with consequences for fruit selection. Neotropical Ornithology 36, 865897.
Moran, C and Catterall, CP (2010) Can functional traits predict ecological interactions? A case study using rain forest frugivores and plants in Australia. Biotropica 42, 318326.
Nooy, W, Mrvar, A and Batagelj, V (2005) Exploratory Social Network Analysis with Pajek. Cambridge: Cambridge University Press, 334 pp.
Olesen, JM, Bascompte, J, Dupont, YL, Elberling, H, Rasmussen, C and Jordano, P (2011) Missing and forbidden links in mutualistic networks. Proceedings of the Royal Society B: Biological Sciences 278, 725732.
Pigot, AL, Bregman, T, Sheard, C, Daly, B, Etienne, RS and Tobias, JA (2016) Quantifying species contributions to ecosystem processes: a global assessment of functional trait and phylogenetic metrics across avian seed-dispersal networks. Proceedings of the Royal Society B: Biological Sciences 283, 20161597.
Ruggera, RA, Blendinger, PG, Gomez, MD and Marshak, C (2016) Linking structure and functionality in mutualistic networks: do core frugivores disperse more seeds than peripheral species? Oikos 125, 541555.
Saracco, JF, Collazo, JA and Groom, MJ (2004) How do frugivores track resources? Insights from spatial analyses of bird foraging in a tropical forest. Oecologia 139, 235245.
Schaefer, HM and Ruxton, GD (2011) Plant–Animal Communication. Oxford: Oxford University Press, 298 pp.
Schaefer, HM and Schmidt, V (2004) Detectability and content as opposing signal characteristics in fruits. Proceedings of the Royal Society of London. Series B: Biological Sciences 271, S370S373.
Schleuning, M, Blüthgen, N, Flörchinger, M, Braun, J, Schaefer, HM and Böhning-Gaese, K (2011) Specialization and interaction strength in a tropical plant-frugivore network differ among forest strata. Ecology 92, 2636.
Schleuning, M, Ingmann, L, Strauß, R, Fritz, SA, Dalsgaard, B, Dehling, DM, Plein, M, Saavedra, F, Sandel, B, Svenning, JC, Böhning-Gaese, K and Dormann, CF (2014) Ecological, historical and evolutionary determinants of modularity in weighted seed-dispersal networks. Ecology letters 17, 454463.
Schmidt, V, Martin Schaefer, H and Winkler, H (2004) Conspicuousness, not colour as foraging cue in plant–animal signalling. Oikos 106, 551557.
Sebastián-González, E, Pires, MM, Donatti, CI, Guimarães, PR and Dirzo, R (2017) Species traits and interaction rules shape a species-rich seed-dispersal interaction network. Ecology and Evolution 7, 44964506.
Snow, DW (1971) Evolutionary aspects of fruit-eating by birds. Ibis 113, 194202.
Stiles, EW (1993) The influence of pulp lipids on fruit preference by birds. Vegetatio 108, 227235.
Sun, C and Moermond, TC (1997) Foraging ecology of three sympatric Turacos in a montane forest in Rwanda. The Auk: Ornithological Advances 114, 396404.
Symonds, MRE and Blomberg, SP (2014) A primer on phylogenetic generalized least squares. In Garamzegi, LZ (ed.), Modern Phylogenetic Comparative Methods and their Application in Evolutionary Biology. New York, NY: Springer, pp. 105130.
Valido, A, Schaefer, HM and Jordano, P (2011) Colour, design and reward: phenotypic integration of fleshy fruit displays. Journal of Evolutionary Biology 24, 751760.
Vanhoni, F and Mendonça, F (2008) O clima do litoral do estado do Paraná. Revista Brasileira de Climatologia 3, 4963.
Venables, WN and Ripley, BD (2002) Modern Applied Statistics with S. (Fourth edition). New York, NY: Springer, 498 pp.
Vizentin-Bugoni, J, Maruyama, PK and Sazima, M (2014) Processes entangling interactions in communities: forbidden links are more important than abundance in a hummingbird-plant network. Proceedings of the Royal Society B 281, 20132397.
Vogel, AI (1989) Titrimetric analysis. In Jeffery, GH, Basset, J, Mendham, J and Denney, C (eds), Vogel’s Textbook of Quantitative Chemical Analysis. Harlow: Longman Scientific and Technical, pp. 372373.
Wheelwright, NT (1985) Fruit-size, gape width, and the diets of fruit-eating birds. Ecology 66, 808818.
Wheelwright, NT and Janson, CH (1985) Colors of fruit displays of bird-dispersed plants in two tropical forests. American Naturalist 126, 777799.
Whelan, CJ, Schmidt, KA, Steele, BB, Quinn, WJ and Dilger, S (1998) Are bird-consumed fruits complementary resources? Oikos 83, 195205.


How do fruit productivity, fruit traits and dietary specialization affect the role of birds in a mutualistic network?

  • Marcia L. Malanotte (a1), Tiago Machado-de-Souza (a1), Ricardo P. Campos (a1), Carmen L.O. Petkowicz (a2) and Isabela G. Varassin (a3)...


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed.