Advertisement

Oecologia

pp 1–13 | Cite as

Local drivers of the structure of a tropical bird-seed dispersal network

  • Tiago Machado-de-SouzaEmail author
  • Ricardo Pamplona Campos
  • Mariano Devoto
  • Isabela Galarda Varassin
Plant-microbe-animal interactions - original research

Abstract

One of the major challenges in ecology is to understand the relative importance of neutral- and niche-based processes structuring species interactions within communities. The concept of neutral-based processes posits that network structure is a result of interactions between species based on their abundance. On the other hand, niche-based processes presume that network structure is shaped by constraints to interactions. Here, we evaluated the relative importance of neutral-based process, represented by species’ abundance (A) and fruit production (F) models, and niche-based process, represented by spatial overlap (S), temporal overlap (T) and morphological barrier (M) models, in shaping the structure of a bird-seed dispersal network from the Brazilian Atlantic Forest. We evaluated the ability of each model, singly or in combination, to predict the general structure [represented by connectance, nestedness (NODF), weight nestedness (WNODF), interaction evenness and complementary specialization] and microstructure of the network (i.e., the frequency of pairwise interactions). Only nestedness (both NODF and WNODF) was predicted by at least one model. NODF and WNODF were predicted by a neutral-based process (A), by a combination of niche-based processes (ST and STM) and by both neutral- and niche-based processes (AM). NODF was also predicted by F and FM model. Regarding microstructure, temporal overlap (T) was the most parsimonious model able to predict it. Our findings reveal that a combination of neutral- and niche-based processes is a good predictor of the general structure (NODF and WNODF) of the bird-seed dispersal network and a niche-based process is the best predictor of the network’s microstructure.

Keywords

Atlantic forest Forbidden links Frugivory Mutualistic network Neutrality 

Notes

Acknowledgements

We thank Fundação Grupo Boticário de Proteção à Natureza (FGBPN) and Sociedade de Pesquisa em Vida Selvagem e Educação Ambiental (SPVS) for field work research permission at RNSM and RNSI; Mater Natura - Instituto de Estudos Ambientais, especially Helena Zarantonieli and Paulo Pizzi, for administrative support; Marcia Malanotte, for help with the field work and Thais B. Zanata for comments on an earlier version of the paper.

Author contribution statement

TMS, RPC and IGV conceived the ideas and designed methodology; TMS and RPC collected the data; TMS analyzed the data and led the writing of the manuscript with support from MD and IGV. All authors contributed critically to the drafts and gave final approval for publication.

Funding

This project was funded by Fundação Grupo Boticário de Proteção à Natureza (FGBPN, project number: 0875); CAPES (scholarships to TM-de-S and RPC and BEX Grant 8971/11-0 to IGV) and CNPq (PQ scholarship 309453/2013-5 to IGV). This study is part of the PhD dissertation of TM-de-S at the Pós-Graduação em Ecologia e Conservação, Universidade Federal do Paraná.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

442_2018_4322_MOESM1_ESM.pdf (1.1 mb)
Supplementary material 1 (PDF 1171 kb)
442_2018_4322_MOESM2_ESM.xlsx (214 kb)
Supplementary material 2 (XLSX 214 kb)

References

  1. Almeida-Neto M, Ulrich W (2011) A straightforward computational approach for measuring nestedness using quantitative matrices. Environ Model Softw 26:173–178.  https://doi.org/10.1016/j.envsoft.2010.08.003 CrossRefGoogle Scholar
  2. Almeida-Neto M, Campassi F, Galetti M et al (2008a) Vertebrate dispersal syndromes along the Atlantic forest: broad-scale patterns and macroecological correlates. Glob Ecol Biogeogr 17:503–513.  https://doi.org/10.1111/j.1466-8238.2008.00386.x CrossRefGoogle Scholar
  3. Almeida-Neto M, Guimarães P, Guimarães PRJ et al (2008b) A consistent metric for nestedness analysis in ecological systems: reconciling concept and measurement. Oikos 117:1227–1239.  https://doi.org/10.1111/j.2008.0030-1299.16644.x CrossRefGoogle Scholar
  4. Bascompte J, Jordano P (2007) Plant-animal mutualistic networks: the architecture of biodiversity. Annu Rev Ecol Evol Syst 38:567–593.  https://doi.org/10.1146/annurev.ecolsys.38.091206.095818 CrossRefGoogle Scholar
  5. Bascompte J, Jordano P (2014) Mutualistic networks. Princeton University Press, PrincetonGoogle Scholar
  6. Bascompte J, Jordano P, Melián CJ, Olesen JM (2003) The nested assembly of plant—animal mutualistic networks. PNAS 100:9383–9387.  https://doi.org/10.1073/pnas.1633576100 CrossRefPubMedGoogle Scholar
  7. Bibby CJ, Burges ND, Hill DA (1992) Bird census techniques, 1st edn. Academic Press, San DiegoGoogle Scholar
  8. Blendinger PG, Ruggera RA, Núñez Montellano MG et al (2012) Fine-tuning the fruit-tracking hypothesis: spatiotemporal links between fruit availability and fruit consumption by birds in Andean mountain forests. J Anim Ecol 81:1298–1310.  https://doi.org/10.1111/j.1365-2656.2012.02011.x CrossRefPubMedGoogle Scholar
  9. Blendinger PG, Giannini NP, Zampini IC et al (2015) Nutrients in fruits as determinants of resource tracking by birds. Ibis (Lond 1859) 157:480–495.  https://doi.org/10.1111/ibi.12274 CrossRefGoogle Scholar
  10. Blüthgen N, Menzel F, Blüthgen N (2006) Measuring specialization in species interaction networks. BMC Ecol 6:9.  https://doi.org/10.1186/1472-6785-6-9 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Blüthgen N, Menzel F, Hovestadt T et al (2007) Specialization, constraints, and conflicting interests in mutualistic networks. Curr Biol 17:341–346.  https://doi.org/10.1016/j.cub.2006.12.039 CrossRefPubMedGoogle Scholar
  12. Burns KC (2006) A simple null model predicts fruit frugivore interactions in a temperate rainforest. Oikos 115:427–432.  https://doi.org/10.1111/j.2006.0030-1299.15068.x CrossRefGoogle Scholar
  13. Burns KC (2013) What causes size coupling in fruit–frugivore interaction webs? Ecology 94:295–300CrossRefGoogle Scholar
  14. Butt N, Seabrook L, Maron M et al (2015) Cascading effects of climate extremes on vertebrate fauna through changes to low-latitude tree flowering and fruiting phenology. Glob Chang Biol 21:3267–3277.  https://doi.org/10.1111/gcb.12869 CrossRefPubMedGoogle Scholar
  15. Chapman CA, Chapman LJ, Wrangham R et al (1992) Estimators of fruit abundance of tropical trees. Biotropica 24:527–531.  https://doi.org/10.2307/2389015 CrossRefGoogle Scholar
  16. Cipollini ML, Levey DJ (1997) Secondary metabolites of fleshy vertebrate-dispersed fruits: adaptive hypotheses and implications for seed dispersal. Am Nat 150:346–372.  https://doi.org/10.1086/286069 CrossRefPubMedGoogle Scholar
  17. Dalsgaard B, Schleuning M, Maruyama PK et al (2017) Opposed latitudinal patterns of network-derived and dietary specialization in avian plant–frugivore interaction systems. Ecography (Cop) 40:1395–1401.  https://doi.org/10.1111/ecog.02604 CrossRefGoogle Scholar
  18. Devoto M, Bailey S, Memmott J (2011) The “night shift”: nocturnal pollen-transport networks in a boreal pine forest. Ecol Entomol 36:25–35.  https://doi.org/10.1111/j.1365-2311.2010.01247.x CrossRefGoogle Scholar
  19. Devoto M, Bailey S, Craze P, Memmott J (2012) Understanding and planning ecological restoration of plant-pollinator networks. Ecol Lett 15:319–328.  https://doi.org/10.1111/j.1461-0248.2012.01740.x CrossRefPubMedGoogle Scholar
  20. Dupont YL, Hansen DM, Olesen JM (2003) Structure of a plant–flower-visitor network in the high-altitude sub-alpine desert of Tenerife, Canary Islands. Ecography (Cop) 26:301–310.  https://doi.org/10.1034/j.1600-0587.2003.03443.x CrossRefGoogle Scholar
  21. Eklöf A, Jacob U, Kopp J et al (2013) The dimensionality of ecological networks. Ecol Lett 16:577–583.  https://doi.org/10.1111/ele.12081 CrossRefPubMedGoogle Scholar
  22. Encinas-Viso F, Revilla TA, Etienne RS (2012) Phenology drives mutualistic network structure and diversity. Ecol Lett 15:198–208.  https://doi.org/10.1111/j.1461-0248.2011.01726.x CrossRefPubMedGoogle Scholar
  23. Fagan WF, Bewick S, Cantrell S et al (2014) Phenologically explicit models for studying plant-pollinator interactions under climate change. Theor Ecol 7:289–297.  https://doi.org/10.1007/s12080-014-0218-8 CrossRefGoogle Scholar
  24. Fitter AH, Fitter RSR (2002) Rapid changes in flowering time in British plants. Science 296:1689–1691.  https://doi.org/10.1126/science.1071617 CrossRefPubMedGoogle Scholar
  25. Flörchinger M, Braun J, Böhning-Gaese K, Schaefer HM (2010) Fruit size, crop mass, and plant height explain differential fruit choice of primates and birds. Oecologia 164:151–161.  https://doi.org/10.1007/s00442-010-1655-8 CrossRefPubMedGoogle Scholar
  26. Gaston KJ, Blackburn TM, Lawton JH (1997) Interspecific abundance-range size relationships: an appraisal of mechanisms. J Anim Ecol 66:579–601.  https://doi.org/10.2307/5951 CrossRefGoogle Scholar
  27. Gonzalez O, Loiselle BA (2016) Species interactions in an Andean bird–flowering plant network: phenology is more important than abundance or morphology. PeerJ 4:e2789.  https://doi.org/10.7717/peerj.2789 CrossRefPubMedPubMedCentralGoogle Scholar
  28. González-Castro A, Yang S, Nogales M, 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 7:1–10.  https://doi.org/10.1093/aobpla/plv017 CrossRefGoogle Scholar
  29. Guimarães PR, Ico-Gray V, dos Reis SF, Thompson JN (2006) Asymmetries in specialization in ant-plant mutualistic networks. Proc R Soc B 273:2041–2047.  https://doi.org/10.1098/rspb.2006.3548 CrossRefPubMedGoogle Scholar
  30. He F, Gaston KJ (2000) Occupancy-abundance relationships and sampling scales. Ecography (Cop) 23:503–511.  https://doi.org/10.1111/j.1600-0587.2000.tb00306.x CrossRefGoogle Scholar
  31. Jordano P (1987) Patterns of mutualistic interactions in pollination and seed dispersal: connectance, dependence asymmetries, and coevolution. Am Nat 129:657–677CrossRefGoogle Scholar
  32. Jordano P, Bascompte J, Olesen JM (2003) Invariant properties in coevolutionary networks of plant-animal interactions. Ecol Lett 6:69–81.  https://doi.org/10.1046/j.1461-0248.2003.00403.x CrossRefGoogle Scholar
  33. Jordano P, Forget P-M, Lambert JE et al (2011) Frugivores and seed dispersal: mechanisms and consequences for biodiversity of a key ecological interaction. Biol Lett 7:321–323.  https://doi.org/10.1098/rsbl.2010.0986 CrossRefPubMedGoogle Scholar
  34. Junker RR, Höcherl N, Blüthgen N (2010) Responses to olfactory signals reflect network structure of flower-visitor interactions. J Anim Ecol 79:818–823.  https://doi.org/10.1111/j.1365-2656.2010.01698.x CrossRefPubMedGoogle Scholar
  35. Kaiser-Bunbury CN, Vázquez DP, Stang M, Ghazoul J (2014) Determinants of the microstructure of plant-pollinator networks. Ecology 95:3314–3324.  https://doi.org/10.1890/14-0024.1.sm CrossRefGoogle Scholar
  36. Kauano EE, Torezan JMD, Cardoso FCG, Marques MCM (2012) Landscape structure in the northern coast of Paraná state, a hotspot for the Brazilian Atlantic Forest conservation. Rev Árvore 36:961–970.  https://doi.org/10.1590/S0100-67622012000500018 CrossRefGoogle Scholar
  37. Krishna A, Guimarães JPR, Jordano P, Bascompte J (2008) A neutral-niche theory of nestedness in mutualistic networks. Oikos 117:1609–1618.  https://doi.org/10.1111/j.1600-0706.2008.16540.x CrossRefGoogle Scholar
  38. Levey DJ (1988) Spatial and temporal variation in Costa Rican fruit and fruit-eating bird abundance. Ecol Monogr 58:251–269CrossRefGoogle Scholar
  39. Loiselle BA, Blake JG (1993) Spatial distribution of understory fruit-eating birds and fruiting plants in a neotropical lowland wet forest. Vegetatio 107:177–189Google Scholar
  40. Maruyama PK, Vizentin-Bugoni J, Oliveira GM et al (2014) Morphological and spatio-temporal mismatches shape a neotropical savanna plant-hummingbird network. Biotropica 46:740–747.  https://doi.org/10.1111/btp.12170 CrossRefGoogle Scholar
  41. Mello MAR, Rodrigues FA, da Costa L, Marquitti FM et al (2015) Keystone species in seed dispersal networks are mainly determined by dietary specialization. Oikos 124:1031–1039.  https://doi.org/10.1111/oik.01613 CrossRefGoogle Scholar
  42. Moermond TC, Denslow JS (1985) Neotropical avian frugivores: patterns of behavior, morphology, and nutrition, with consequences for fruit selection. Ornithol Monogr 36:865–897CrossRefGoogle Scholar
  43. Olesen JM, Bascompte J, Dupont YL et al (2010) Missing and forbidden links in mutualistic networks. Proc R Soc B Biol Sci 278:725–732.  https://doi.org/10.1098/rspb.2010.1371 CrossRefGoogle Scholar
  44. Olito C, Fox JW (2014) Species traits and abundances predict metrics of plant-pollinator network structure, but not pairwise interactions. Oikos 124:428–436.  https://doi.org/10.1111/oik.01439 CrossRefGoogle Scholar
  45. Petchey OL, Gaston KJ (2002) Functional diversity (FD), species richness and community composition. Ecol Lett 5:402–411.  https://doi.org/10.1046/j.1461-0248.2002.00339.x CrossRefGoogle Scholar
  46. Pizo MA, Galetti M (2010) Métodos e Perspectivas da Frugivoria e Dispersão de Sementes por Aves. In: Von Matter S, Straube FC, de Piacentini VQ (eds) Ornitologia e Conservação: Ciência Aplicada, Técnicas de Pesquisa e Levantamento. Technical Books Editoria, Rio de Janeiro, pp 491–504Google Scholar
  47. R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 4 Aug 2017
  48. Santamaría L, Rodríguez-Gironés MA (2007) Linkage rules for plant-pollinator networks: trait complementarity or exploitation barriers? PLoS Biol 5:354–362.  https://doi.org/10.1371/journal.pbio.0050031.t001 CrossRefGoogle Scholar
  49. Sazatornil FD, Moré M, Benitez-Vieyra S et al (2016) Beyond neutral and forbidden links: morphological matches and the assembly of mutualistic hawkmoth-plant networks. J Anim Ecol 85:1586–1594.  https://doi.org/10.1111/1365-2656.12509 CrossRefPubMedGoogle Scholar
  50. Schleuning M, Blüthgen N, Flörchinger M et al (2011) Specialization and interaction strength in a tropical plant-frugivore network differ among forest strata. Ecology 92:26–36CrossRefGoogle Scholar
  51. Sebastián-González E (2017) Drivers of species role in avian seed-dispersal mutualistic networks. J Anim Ecol 38:42–49.  https://doi.org/10.1111/ijlh.12426 CrossRefGoogle Scholar
  52. Stang M, Klinkhamer PGL, van der Meijden E (2007) Asymmetric specialization and extinction risk in plant–flower visitor webs: a matter of morphology or abundance? Oecologia 151:442–453.  https://doi.org/10.1007/s00442-006-0585-y CrossRefPubMedGoogle Scholar
  53. Sun C, Moermond TC (1997) Foraging ecology of three sympatric Turacos in a montane forest in Rwanda. Auk 114:396–404.  https://doi.org/10.2307/4089241 CrossRefGoogle Scholar
  54. Tylianakis JM, Tscharntke T, Lewis OT (2007) Habitat modification alters the structure of tropical host–parasitoid food webs. Nature 445:202–205.  https://doi.org/10.1038/nature05429 CrossRefPubMedGoogle Scholar
  55. Vanhoni F, Mendonça F (2008) O clima do litoral do estado do Paraná. Rev Bras Climatoli 3:49–63Google Scholar
  56. Vázquez DP, Melián CJ, Williams NM et al (2007) Species abundance and asymmetric interaction strength in ecological networks. Oikos 116:1120–1127.  https://doi.org/10.1111/j.2007.0030-1299.15828.x CrossRefGoogle Scholar
  57. Vázquez DP, Chacoff NP, Cagnolo L (2009) Evaluating multiple determinants of the structure of plant–animal mutualistic networks. Ecology 90:2039–2046.  https://doi.org/10.1890/08-1837.1 CrossRefPubMedGoogle Scholar
  58. Vielliard JME, Almeida MEC et al (2010) Levantamento quantitativo por pontos de escuta e o Índice Pontual de Abundância (IPA). In: Von Matter S, Straube FC, de Piacentini VQ (eds) Ornitologia e Conservação: Ciência Aplicada, Técnicas de Pesquisa e Levantamento. Technical Books Editoria, Rio de Janeiro, pp 45–60Google Scholar
  59. Vizentin-Bugoni J, Maruyama PK, Sazima M (2014) Processes entangling interactions in communities: forbidden links are more important than abundance in a hummingbird-plant network. Proc R Soc B 281:20132397.  https://doi.org/10.1098/rspb.2013.2397 CrossRefPubMedGoogle Scholar
  60. Vizentin-Bugoni J, Maruyama PK, de Souza CS et al (2018) Plant-pollinator networks in the tropics: a review. In: Dátillo W, Rico-Gray V (eds) Ecological networks in the tropics: an integrative overview of species interactions from some of the most species-rich habitats on earth. Springer, Switzerland, pp 73–91CrossRefGoogle Scholar
  61. Wheelwright N (1985) Fruit-size, gape width, and the diets of fruit-eating birds. Ecology 66:808–818CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Laboratório de Interações e Biologia ReprodutivaDepartamento de Botânica, Universidade Federal do Paraná, Centro PolitécnicoCuritibaBrazil
  2. 2.Programa de Pós-Graduação em Ecologia e ConservaçãoUniversidade Federal do Paraná, Centro PolitécnicoCuritibaBrazil
  3. 3.Mater Natura-Instituto de Estudos AmbientaisCuritibaBrazil
  4. 4.Instituto de Estudos Ambientais do Paraná (IEAP)CuritibaBrazil
  5. 5.Facultad de Agronomía, Cátedra de Botánica GeneralUniversidad de Buenos AiresBuenos AiresArgentina
  6. 6.Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)Buenos AiresArgentina

Personalised recommendations