Advertisement

Oecologia

pp 1–11 | Cite as

Direct and indirect effects of plant and frugivore diversity on structural and functional components of fruit removal by birds

  • Marta QuitiánEmail author
  • Vinicio Santillán
  • Carlos Iván Espinosa
  • Jürgen Homeier
  • Katrin Böhning-Gaese
  • Matthias Schleuning
  • Eike Lena Neuschulz
Plant-microbe-animal interactions - original research

Abstract

Seed dispersal is an important ecosystem function, but it is contentious how structural and functional diversity of plant and bird communities are associated with seed-dispersal functions. We used structural equation models to test how structural (i.e., abundance, species richness) and functional diversity (i.e., functional dispersion and community-weighted means of functional traits) of fruiting plants and frugivorous birds directly and indirectly influence the respective components of fruit removal. We recorded plant and bird diversity in point counts and observed plant–frugivore interactions in a tropical mountain forest in Ecuador. We also recorded plant and bird morphological traits to calculate measures of functional diversity. We found that fruit abundance had a positive direct effect on bird abundance, which directly and indirectly mediated the abundance of removed fruits. Plant and bird species richness were only directly related to the richness of the removed fruits. Functional dispersion of the plant community was positively associated to that of the bird community and to that of the removed fruits. Consistently, we found positive associations between community-weighted means of plant and bird traits and between community-weighted means of plant traits and that of plants with removed fruits. In contrast, community-weighted means of the bird community were unrelated to that of the removed fruits. Overall, our results suggest that plant abundance directly and indirectly influences fruit removal, likely because of avian fruit tracking. However, we did not find strong links between the functional diversity of the frugivore community and removed fruits, suggesting that other factors in addition to plant–animal trait matching might be important for the functional diversity of removed fruits. Our findings highlight the importance of frugivore abundance for maintaining seed dispersal by animals in tropical forests.

Keywords

Seed dispersal Plant–frugivore interaction networks Functional trait diversity Species identity Structural equation models Tropical montane forest 

Notes

Acknowledgements

We thank the German Research Foundation (DFG) for funding our projects in the framework of the Research Bundle 823–825 “Platform for Biodiversity and Ecosystem Monitoring and Research in South Ecuador” (PAK 825/1) and the Research Unit FOR2730 “Environmental changes in biodiversity hotspot ecosystems of South Ecuador: RESPonse and feedback effECTs”. The Ecuadorian Ministry of the Environment (MAE) kindly provided permission to conduct research. We thank Nature and Culture International (NCI), Felix Matt, Jörg Zeilinger and Catherine Vits for logistic support. We are grateful to Agustín Carrasco, Patricio Estrella, Dagmar Hanz and Nina Gunselmann for their help in fieldwork. We thank Dagmar Hanz, Larissa Nowak and Anna Phillips for their help measuring bird traits. Three anonymous reviewers provided valuable comments on an earlier version of this manuscript.

Author contribution statement

MS, ELN, KBG, MQ, VS conceived and designed the study. MQ and VS collected the data. JH identified the botanical samples. MQ analyzed the data. MQ, MS, ELN led the writing of the manuscript with editorial advice from KBG, JH and CIE.

Supplementary material

442_2018_4324_MOESM1_ESM.doc (85 kb)
Supplementary material 1 (DOC 85 kb)

References

  1. Albrecht J, Berens DG, Blüthgen N et al (2013) Logging and forest edges reduce redundancy in plant–frugivore networks in an old-growth European forest. J Ecol 101:990–999.  https://doi.org/10.1111/1365-2745.12105 CrossRefGoogle Scholar
  2. Balbanera P, Pfisterer AB, Buchmann N et al (2006) Quantifying the evidence for biodiversity effects on ecosystem functioning and services. Ecol Lett 9:1146–1156.  https://doi.org/10.1111/j.1461-0248.2006.00963.x CrossRefGoogle Scholar
  3. Bender IMA, Kissling WD, Katrin B et al (2017) Functionally specialised birds respond flexibly to seasonal changes in fruit availability. J Anim Ecol 86:800–811.  https://doi.org/10.1111/1365-2656.12683 CrossRefPubMedGoogle Scholar
  4. Bender IMA, Kissling WD, Blendinger PG et al (2018) Morphological trait matching shapes plant–frugivore networks across the Andes. Ecography.  https://doi.org/10.1111/ecog.03396 CrossRefGoogle Scholar
  5. Bendix J, Rollenbeck RT, Richter M et al (2008) Climate Variability. In: Beck EH, Bendix J, Kottke IL et al (eds) Gradients in a tropical mountain ecosystem of Ecuador. Springer, Heidelberg, pp 63–73CrossRefGoogle Scholar
  6. Blendinger PG, Villegas M (2011) Crop size is more important than neighborhood fruit availability for fruit removal of Eugenia uniflora (Myrtaceae) by bird seed dispersers. Plant Ecol 212:889–899.  https://doi.org/10.1007/s11258-010-9873-z CrossRefGoogle Scholar
  7. Cardinale BJ, Srivastava DS, Duffy JE et al (2006) Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989–992.  https://doi.org/10.1038/nature05202 CrossRefPubMedGoogle Scholar
  8. Chapin FS, Zavaleta ES, Eviner VT et al (2000) Consequences of changing biodiversity. Nature 405:234–242.  https://doi.org/10.1038/35012241 CrossRefPubMedGoogle Scholar
  9. Chave J (2004) Neutral theory and community ecology. Ecol Lett 7:241–253.  https://doi.org/10.1111/j.1461-0248.2003.00566.x CrossRefGoogle Scholar
  10. Dehling DM, Fritz SA, Töpfer T et al (2014a) Functional and phylogenetic diversity and assemblage structure of frugivorous birds along an elevational gradient in the tropical Andes. Ecography 37:1047–1055.  https://doi.org/10.1111/ecog.00623 CrossRefGoogle Scholar
  11. Dehling DM, Töpfer T, Schaefer HM et al (2014b) Functional relationships beyond species richness patterns: trait matching in plant–bird mutualisms across scales. Glob Ecol Biogeogr 23:1085–1093.  https://doi.org/10.1111/geb.12193 CrossRefGoogle Scholar
  12. Dehling DM, Jordano P, Schaefer HM et al (2016) Morphology predicts species’ functional roles and their degree of specialization in plant–frugivore interactions. Proc B 283:20152444.  https://doi.org/10.1098/rspb.2015.2444 CrossRefGoogle Scholar
  13. Dias ATC, Berg MP, de Bello F et al (2013) An experimental framework to identify community functional components driving ecosystem processes and services delivery. J Ecol 101:29–37.  https://doi.org/10.1111/1365-2745.12024 CrossRefGoogle Scholar
  14. Donoso I, García D, Martínez D et al (2017) Complementary effects of species abundances and ecological neighborhood on the occurrence of fruit–frugivore interactions. Front Ecol Evol 5:1–12.  https://doi.org/10.3389/fevo.2017.00133 CrossRefGoogle Scholar
  15. Duffy JE (2009) Why biodiversity is important to the functioning of real-world ecosystems. Front Ecol Environ 7:437–444.  https://doi.org/10.1890/070195 CrossRefGoogle Scholar
  16. Dunning JJB (2007) CRC handbook of avian body masses, 2nd edn. Taylor & Francis, Boca RatonCrossRefGoogle Scholar
  17. Eshiamwata GW, Berens DG, Bleher B et al (2006) Bird assemblages in isolated Ficus trees in Kenyan farmland. J Trop Ecol 22:723–726.  https://doi.org/10.1017/S0266467406003646 CrossRefGoogle Scholar
  18. Ferger SW, Schleuning M, Hemp A et al (2014) Food resources and vegetation structure mediate climatic effects on species richness of birds. Glob Ecol Biogeogr 23:541–549.  https://doi.org/10.1111/geb.12151 CrossRefGoogle Scholar
  19. Fleming TH (1979) Do tropical frugivores compete for food? Am Zool 19:1157–1172.  https://doi.org/10.1093/icb/19.4.1157 CrossRefGoogle Scholar
  20. Fontaine C, Dajoz I, Meriguet J, Loreau M (2006) Functional diversity of plant–pollinator interaction webs enhances the persistence of plant communities. PLoS Biol 4:129–135.  https://doi.org/10.1371/journal.pbio.0040001 CrossRefGoogle Scholar
  21. Gagic V, Bartomeus I, Jonsson T et al (2015) Functional identity and diversity of animals predict ecosystem functioning better than species-based indices. Proc R Soc B Biol Sci 282:20142620.  https://doi.org/10.1098/rspb.2014.2620 CrossRefGoogle Scholar
  22. García D, Martínez D (2012) Species richness matters for the quality of ecosystem services: a test using seed dispersal by frugivorous birds. Proc R Soc B Biol Sci 279:3106–3113.  https://doi.org/10.1098/rspb.2012.0175 CrossRefGoogle Scholar
  23. García D, Zamora R, Amico GC (2010) Birds as suppliers of seed dispersal in temperate ecosystems: conservation guidelines from real-world landscapes. Conserv Biol 24:1070–1079.  https://doi.org/10.1111/j.1523-1739.2009.01440.x CrossRefPubMedGoogle Scholar
  24. Grime JP (1998) Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J Ecol 86:902–910.  https://doi.org/10.1046/j.1365-2745.1998.00306.x CrossRefGoogle Scholar
  25. Grime JP, Thompson K, Hunt R et al (1997) Integrated screening validates primary axes of specialisation in plants. Oikos 79:259–281CrossRefGoogle Scholar
  26. Hooper DU, Chapin FS, Ewel JJ et al (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35.  https://doi.org/10.1890/04-0922 CrossRefGoogle Scholar
  27. Howe HF, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Syst 13:201–228CrossRefGoogle Scholar
  28. Jetz W, Kreft H, Ceballos G, Mutke J (2009) Global associations between terrestrial producer and vertebrate consumer diversity. Proc R Soc B Biol Sci 276:269–278.  https://doi.org/10.1098/rspb.2008.1005 CrossRefGoogle Scholar
  29. Jordano P, Schupp EW (2000) Seed disperser effectiveness: the quantity component and patterns of seed rain for Prunus mahaleb. Ecol Monogr 70:591–615.  https://doi.org/10.1890/0012-9615(2000)070%5b0591:sdetqc%5d2.0.co;2 CrossRefGoogle Scholar
  30. Kembel SW, Cowan PD, Helmus MR et al (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464CrossRefGoogle Scholar
  31. Laliberté E, Legendre P (2010) A distance-based framework for measuring from multiple traits functional diversity. Ecology 91:299–305.  https://doi.org/10.1890/08-2244.1 CrossRefPubMedGoogle Scholar
  32. Lavorel S, Grigulis K, Lamarque P et al (2011) Using plant functional traits to understand the landscape distribution of multiple ecosystem services. J Ecol 99:135–147.  https://doi.org/10.1111/j.1365-2745.2010.01753.x CrossRefGoogle Scholar
  33. Leibold MA, McPeek MA (2006) Coexistence of the niche and neutral perspectives in community ecology. Ecology 87:1399–1410.  https://doi.org/10.1890/0012-9658(2006)87%5b1399:cotnan%5d2.0.co;2 CrossRefPubMedGoogle Scholar
  34. Loiselle BA, Blake JG (1991) Temporal variation in birds and fruits along an elevational gradient in Costa Rica. Ecology 72:180–193.  https://doi.org/10.2307/1938913 CrossRefGoogle Scholar
  35. Loreau M (2000) Biodiversity and ecosystem functioning: recent theoretical advances. Oikos 91:3–17.  https://doi.org/10.1034/j.1600-0706.2000.910101.x CrossRefGoogle Scholar
  36. Loreau M (2001) Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–808.  https://doi.org/10.1126/science.1064088 CrossRefPubMedGoogle Scholar
  37. Maglianesi MA, Blüthgen N, Böhning-gaese K, Schleuning M (2015) Functional structure and specialization in three tropical plant–hummingbird interaction networks across an elevational gradient in Costa Rica. Ecography 38:1119–1128.  https://doi.org/10.1111/ecog.01538 CrossRefGoogle Scholar
  38. Mayfield MM, Bonser SP, Morgan JW et al (2010) What does species richness tell us about functional trait diversity? Predictions and evidence for responses of species and functional trait diversity to land-use change. Glob Ecol Biogeogr 19:423–431.  https://doi.org/10.1111/j.1466-8238.2010.00532.x CrossRefGoogle Scholar
  39. McCain CM, Grytnes J (2010) Elevational gradients in species richness. In: Jonsson R (ed) Encyclopedia of life sciences. Wiley, Chichester, pp 1–10Google Scholar
  40. McCollin D, Moore L, Sparks T (2000) The flora of a cultural landscape: environmental determinants of change revealed using archival sources. Biol Conserv 92:249–263.  https://doi.org/10.1016/S0006-3207(99)00070-1 CrossRefGoogle Scholar
  41. Menke S, Böhning-Gaese K, Schleuning M (2012) Plant–frugivore networks are less specialized and more robust at forest–farmland edges than in the interior of a tropical forest. Oikos 121:1553–1566.  https://doi.org/10.1111/j.1600-0706.2011.20210.x 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. Moser G, Hertel D, Leuschner C et al (2007) Altitudinal change in a LAI and stand leaf biomass in tropical montane forest: a transect study in Ecuador and a pan-tropical meta-analysis. Ecosytems 10:924–935.  https://doi.org/10.1007/sl0021-007-9063-6 CrossRefGoogle Scholar
  44. Muñoz MC, Schaefer HM, Böhning-Gaese K, Schleuning M (2017a) Importance of animal and plant traits for fruit removal and seedling recruitment in a tropical forest. Oikos 126:823–832.  https://doi.org/10.1111/oik.03547 CrossRefGoogle Scholar
  45. Muñoz MC, Schaefer HM, Böhning-Gaese K, Schleuning M (2017b) Positive relationship between fruit removal by animals and seedling recruitment in a tropical forest. Basic Appl Ecol 20:31–39.  https://doi.org/10.1016/j.baae.2017.03.001 CrossRefGoogle Scholar
  46. Naeem S, Wright JP (2003) Disentangling biodiversity effects on ecosystem functioning: deriving solutions to a seemingly insurmountable problem. Ecol Lett 6:567–579.  https://doi.org/10.1046/j.1461-0248.2003.00471.x CrossRefGoogle Scholar
  47. Neuschulz EL, Botzat A, Farwig N (2011) Effects of forest modification on bird community composition and seed removal in a heterogeneous landscape in South Africa. Oikos 120:1371–1379.  https://doi.org/10.1111/j.1600-0706.2011.19097.x CrossRefGoogle Scholar
  48. Neuschulz EL, Brown M, Farwig N (2013) Frequent bird movements across a highly fragmented landscape: the role of species traits and forest matrix. Anim Conserv 16:170–179.  https://doi.org/10.1111/j.1469-1795.2012.00582.x CrossRefGoogle Scholar
  49. Neuschulz EL, Mueller T, Schleuning M, Böhning-Gaese K (2016) Pollination and seed dispersal are the most threatened processes of plant regeneration. Sci Rep 6:29839.  https://doi.org/10.1038/srep29839 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Plein M, Längsfeld L, Neuschulz EL et al (2013) Constant properties of plant–frugivore networks despite fluctuations in fruit and bird communities in space and time. Ecology 94:1296–1306.  https://doi.org/10.1890/12-1213.1 CrossRefPubMedGoogle Scholar
  51. Rosseel Y (2012) Lavaan: an R package for structural equation modeling and more Version 0.5–12 (BETA). J Statistical software 48:1–36CrossRefGoogle Scholar
  52. Saavedra F, Hensen I, Beck SG et al (2014) Functional importance of avian seed dispersers changes in response to human-induced forest edges in tropical seed-dispersal networks. Oecologia 176:837–848.  https://doi.org/10.1007/s00442-014-3056-x CrossRefPubMedGoogle Scholar
  53. Santillán VE, Quitián M, Tinoco BA et al (2018) Spatio-temporal variation in bird assemblages is associated with fluctuations in temperature and precipitation along a tropical elevational gradient. PLoS One 13:e0196179.  https://doi.org/10.1371/journal.pone.0196179 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Schleuning M, Fründ J, García D (2015) Predicting ecosystem functions from biodiversity and mutualistic networks: an extension of trait-based concepts to plant–animal interactions. Ecography 38:380–392.  https://doi.org/10.1111/ecog.00983 CrossRefGoogle Scholar
  55. Tilman D (2001) Functional diversity. In: Levin SA (ed) Encyclopedia of biodiversity. Academic Press, San Diego, CA, pp 109–120CrossRefGoogle Scholar
  56. Violle C, Navas M, Vile D et al (2007) Let the concept of trait be functional! Oikos 116:882–892.  https://doi.org/10.1111/j.0030-1299.2007.15559 CrossRefGoogle Scholar
  57. Vollstädt MGR, Ferger SW, Hemp A et al (2017) Direct and indirect effects of climate, human disturbance and plant traits on avian functional diversity. Glob Ecol Biogeogr 2017:1–10.  https://doi.org/10.1111/geb.12606 CrossRefGoogle Scholar
  58. Wheelwright NT (1985) Fruit-size, gape width, and the diets of fruit-eating birds. Ecology 66:808–818CrossRefGoogle Scholar
  59. Wilman H, Belmaker J, Simpson J, de la Rosa C et al (2014) EltonTraits 1.0: species-level foraging attributes of the world’s birds and mammals. Ecology 95:2027.  https://doi.org/10.1890/13-1917.1 CrossRefGoogle Scholar
  60. Winfree R, Fox JW, Williams NM et al (2015) Abundance of common species, not species richness, drives delivery of a real-world ecosystem service. Ecol Lett 18:626–635.  https://doi.org/10.1111/ele.12424 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Senckenberg Biodiversity and Climate Research Centre FrankfurtFrankfurt am MainGermany
  2. 2.Goethe University FrankfurtFrankfurt am MainGermany
  3. 3.Universidad Técnica Particular de Loja (UTPL)LojaEcuador
  4. 4.Plant Ecology and Ecosystems ResearchUniversity of GöttingenGöttingenGermany

Personalised recommendations