Biodiversity and Conservation

, Volume 26, Issue 12, pp 2803–2819 | Cite as

Assessing the relative importance of isolated Ficus trees to insectivorous birds in an Indian human-modified tropical landscape

  • Thomas J. MatthewsEmail author
  • H. Eden W. Cottee-Jones
  • Tom P. Bregman
  • Robert J. Whittaker
Original Paper


The destruction of forest for agricultural expansion has created a vast estate of human-modified land in tropical regions. One group of organisms that are particularly vulnerable to the loss of forest habitat are insectivorous birds. Despite this, few conservation strategies have been identified for this group in human-modified landscapes. We survey the use of 104 isolated trees by insectivorous birds in rural Assam, India. We used an information theoretic model comparison approach to determine the important variables driving insectivorous bird diversity within these isolated trees. Our work demonstrates that the conservation of large trees in human-modified landscapes may play an important role in maintaining bird diversity and ecological function beyond the forest edge. More specifically, we found that isolated Ficus trees hold assemblages with particularly high insectivore abundance, richness and functional diversity when compared to other isolated fruit and large trees. We argue that, where present, Ficus trees should be actively conserved in human-modified landscapes to maintain the composition of insectivore communities in a “Ficus first” strategy.


Conservation beyond protected areas Birds Ecological function Ficus India Insectivores Isolated trees Multimodel inference 



The authors wish to thank Maan Barua, Manju Barua, Barry and Susan Jones, A.J. Tours and Travel, and Wild Grass Eco Lodge for help facilitating this study. Valuable field assistance was provided by Biju Hazarika, Gokul Munda, Soano Rajbonsi, Raju Gogoi, Nakib Ali, Polash Bora, Colia Karmakar, and Humnot Borah. We are very grateful for advice and comments provided by François Rigal, Michael Børregaard, Richard Grenyer, Paul Jepson, Catherine Sheard, Jon Sadler, Ross Crates and an anonymous reviewer.

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to declare.

Ethical approval

This research was conducted with ethical approval from the University of Oxford (Departmental CUREC reference number: SOGE C1A-99). Surveys were conducted with permission from local landowners where necessary, and permission to conduct this field work in India was granted by the High Commission of India, London, under visa number 4246496. Field studies did not impact the welfare of the animals studied.

Supplementary material

10531_2017_1387_MOESM1_ESM.docx (25 kb)
Supplementary material 1 (DOCX 24 kb)


  1. Azhar B, Lindenmayer DB, Wood J, Fischer J, Manning A, McElhinny C, Zakaria M (2013) The influence of agricultural system, stand structural complexity and landscape context on foraging birds in oil palm landscapes. Ibis 155:297–312CrossRefGoogle Scholar
  2. Bain A, Harrison RD, Schatz B (2013) How to be an ant on figs. Acta Oecol 57:97–108CrossRefGoogle Scholar
  3. Bartoń K (2016) Package ‘MuMIn’: multi-model inference. R package version 1(15):6Google Scholar
  4. Barua M, Sharma P (1999) Birds of Kaziranga National Park, India. Forktail 15:47–60Google Scholar
  5. Basset Y, Novotny V (1999) Species richness of insect herbivore communities on Ficus in Papua New Guinea. Biol J Lin Soc 67:477–499CrossRefGoogle Scholar
  6. Basset Y, Novotny V, Weiblen G (1997) Ficus: a resource for arthropods in the tropics, with particular reference to New Guinea. In: Watt AD, Stork NE, Hunter MD (eds) Forests and insects. Chapman and Hall, London, pp 341–361Google Scholar
  7. Bivand R, Piras G (2015) Comparing implementations of estimation methods for spatial econometrics. J Stat Softw 63:1–36Google Scholar
  8. Bolker B (2016) Dealing with quasi-models in R. Compare 1:5–452305Google Scholar
  9. Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information-theoretic approach. Springer, LondonGoogle Scholar
  10. Champion HG, Seth SK (1968) A revised survey of forest types of India. Government of India Press, New DelhiGoogle Scholar
  11. Chazdon RL, Harvey CA, Komar O, Griffith DM, Ferguson BG, Martínez-Ramos M, Morales H, Nigh R, Soto-Pinto L, van Breugel M, Philpott SM (2009) Beyond reserves: a research agenda for conserving biodiversity in human-modified tropical landscapes. Biotropica 41:142–153CrossRefGoogle Scholar
  12. Claramunt S, Derryberry EP, Remsen JV Jr, Brumfield RT (2012) High dispersal ability inhibits speciation in a continental radiation of passerine birds. Proc R Soc B 279:1567–1574CrossRefPubMedGoogle Scholar
  13. Cottee-Jones HEW, Whittaker RJ (2015) Felling Ficus: the cultural status of fig trees in a rural Assamese community, India. Ethnobiol Lett 6:89–98CrossRefGoogle Scholar
  14. Cottee-Jones HEW, Bajpai O, Chaudhary LB, Whittaker RJ (2015a) Isolated Ficus trees deliver dual conservation and development benefits in a rural landscape. Ambio 44:678–684CrossRefPubMedPubMedCentralGoogle Scholar
  15. Cottee-Jones HEW, Matthews TJ, Bregman TP, Barua M, Tamuly J, Whittaker RJ (2015b) Are protected areas required to maintain functional diversity in human-modified landscapes? PLoS ONE 10:e0123952CrossRefPubMedPubMedCentralGoogle Scholar
  16. Cottee-Jones HEW, Bajpai O, Chaudhary LB, Whittaker RJ (2016) The importance of Ficus (Moraceae) trees for tropical forest restoration. Biotropica 48:413–419CrossRefGoogle Scholar
  17. Cushman JH, Compton SG, Zachariades C, Ware AB, Nefdt RJC, Rashbrook VK (1998) Geographic and taxonomic distribution of a positive interaction: ant-tended homopterans indirectly benefit figs across southern Africa. Oecologia 116:373–380CrossRefPubMedGoogle Scholar
  18. del Hoyo J, Elliott A Sargatal J (1992–2002) Handbook of the birds of the world. Vol. 1–7. Lynx Edicions, BarcelonaGoogle Scholar
  19. del Hoyo J, Elliott A, Christie DA (2003–2011) Handbook of the birds of the world. Vol. 8–16. Lynx Edicions, BarcelonaGoogle Scholar
  20. Derryberry EP, Claramunt S, Derryberry G, Chesser RT, Cracraft J, Alexio A, Pérez-Emán J, Remsen JV Jr, Brumfield RT (2011) Lineage diversification and morphological evolution in a large-scale continental radiation: the Neotropical ovenbirds and woodcreepers (Aves: Furnariidae). Evolution 65:2973–2986CrossRefPubMedGoogle Scholar
  21. Edwards FA, Edwards DP, Hamer KC, Davies RG (2013) Impacts of logging and conversion of rainforest to oil palm on the functional diversity of birds in Sundaland. Ibis 155:313–326CrossRefGoogle Scholar
  22. ESRI (2014) ArcGIS desktop: release 10.2.1. Environmental Systems Research Institute, RedlandsGoogle Scholar
  23. Fischer J, Lindenmayer DB, Manning AD (2006) Biodiversity, ecosystem function, and resilience: ten guiding principles for commodity production landscapes. Front Ecol Environ 4:80–86CrossRefGoogle Scholar
  24. Fischer J, Stott J, Law BS (2010) The disproportionate value of scattered trees. Biol Cons 143:1564–1567CrossRefGoogle Scholar
  25. Flynn FB, Gogol-Prokurat M, Nogeire T, Molinari N, Trautman Richers B, Lin BB, Simpson N, Mayfield MM, DeClerck F (2009) Loss of functional diversity under land use intensification across multiple taxa. Ecol Lett 12:22–33CrossRefPubMedGoogle Scholar
  26. Fox J, Weisberg S (2011) An R companion to applied regression, 2nd edn. Sage, CaliforniaGoogle Scholar
  27. Gardner TA, Barlow J, Chazdon RL, Ewers RM, Harvey CA, Peres CA, Sodhi NS (2009) Prospects for tropical forest biodiversity in a human-modified world. Ecol Lett 12:561–582CrossRefPubMedGoogle Scholar
  28. Giam X, Olden JD (2016) Quantifying variable importance in a multimodel inference framework. Methods Ecol Evol 7:388–397CrossRefGoogle Scholar
  29. Gibbons P, Lindenmayer DB, Fischer J, Manning AD, Weinberg A, Seddon J, Ryan P, Barrett G (2008) The future of scattered trees in agricultural landscapes. Conserv Biol 22:1309–1319CrossRefPubMedGoogle Scholar
  30. Harrison RD (2003) Fig wasp dispersal and the stability of a keystone plant resource in Borneo. Proc R Soc Lond B 270:S76–S79CrossRefGoogle Scholar
  31. Harrison RD (2013) Ecology of a fig ant-plant. Acta Oecol 57:88–96CrossRefGoogle Scholar
  32. Harvey CA, Medina A, Sánchez DM, Vílchez S, Hernández B, Saenz JC, Maes JM, Casanoves F, Sinclair FL (2006) Patterns of animal diversity in different forms of tree cover in agricultural landscapes. Ecol Appl 16:1986–1999CrossRefPubMedGoogle Scholar
  33. IBM (2013) IBM SPSS statistics for windows, Version 2.20. IBM Corp, ArmonkGoogle Scholar
  34. Karp DS, Daily GC (2013) Cascading effects of insectivorous birds and bats in tropical coffee plantations. Ecology 95:1065–1074CrossRefGoogle Scholar
  35. Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305CrossRefPubMedGoogle Scholar
  36. Laliberté E, Shipley B (2013) FD-package. Measuring functional diversity from multiple traits and other tools for functional ecology. Version 1.0–11Google Scholar
  37. Laliberté E, Wells JA, DeClerck F, Metcalfe DJ, Catterall CP, Queiroz C, Aubin I, Bonser SP, Ding Y, Fraterrigo JM, McNamara S, Morgan JW, Merlos DS, Vesk PA, Mayfield MM (2010) Land-use intensification reduces functional redundancy and response diversity in plant communities. Ecol Lett 13:76–86CrossRefPubMedGoogle Scholar
  38. Leighton M, Leighton DR (1983) Vertebrate responses to fruiting seasonality within a Bornean rain forest. In: Sutton SL, Whitmore TC, Chadwick AC (eds) Tropical rain forest: ecology and management. Blackwell, Oxford, pp 181–196Google Scholar
  39. Luck GW, Daily GC (2003) Tropical countryside bird assemblages: richness, composition, and foraging differ by landscape context. Ecol Appl 13:235–247CrossRefGoogle Scholar
  40. Manning AD, Lindenmayer DB, Barry SC (2004) The conservation implications of bird reproduction in the agricultural “matrix”: a case study of the vulnerable superb parrot of south-eastern Australia. Biol Cons 120:363–374CrossRefGoogle Scholar
  41. Manning AD, Fischer J, Lindenmayer DB (2006) Scattered trees are keystone structures—implications for conservation. Biol Cons 132:311–321CrossRefGoogle Scholar
  42. Matthews TJ, Cottee-Jones HEW, Whittaker RJ (2014) Habitat fragmentation and the species–area relationship: a focus on total species richness obscures the impact of habitat loss on habitat specialists. Divers Distrib 20:1136–1146CrossRefGoogle Scholar
  43. McGill BJ, Enquist BJ, Weiher E, Westoby M (2006) Rebuilding community ecology from functional traits. Trends Ecol Evol 21:178–185CrossRefPubMedGoogle Scholar
  44. Melo FPL, Arroyo-Rodríguez V, Fahrig L, Martínez-Ramos M, Tabarelli M (2013) On the hope for biodiversity-friendly tropical landscapes. Trends Ecol Evol 28:462–468CrossRefPubMedGoogle Scholar
  45. Pereira RAS, Semir J, de Oliveira Menezes A Jr (2000) Pollination and other biotic interactions in figs of Ficus eximia Schott (Moraceae). Rev Bras Bot 23:217–224CrossRefGoogle Scholar
  46. Petchey OL, Gaston KJ (2006) Functional diversity: back to basics and looking forward. Ecol Lett 9:741–758CrossRefPubMedGoogle Scholar
  47. Phalan B, Bertzky M, Butchart SHM, Donald PF, Scharlemann JPW, Stattersfield AJ, Balmford A (2013) Crop expansion and conservation priorities in tropical countries. PLoS ONE 8:e51759CrossRefPubMedPubMedCentralGoogle Scholar
  48. R Core Team (2014) R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing. Version 3.0.3Google Scholar
  49. Richards SA (2008) Dealing with overdispersed count data in applied ecology. J Appl Ecol 45:218–227CrossRefGoogle Scholar
  50. Schatz B, Kjellberg F, Nyawa S, Hossaert-McKey M (2008) Fig wasps: a staple food for ants on Ficus. Biotropica 40:190–195CrossRefGoogle Scholar
  51. Schweiger O, Musche M, Bailey D, Billeter R, Diekötter T, Hendrickx F, Herzog F, Liira J, Maelfait J-P, Speelmans M, Dziock F (2007) Functional richness of local hoverfly communities (Diptera, Syrphidae) in response to land use across temperate Europe. Oikos 116:461–472CrossRefGoogle Scholar
  52. Şekercioğlu CH (2012) Bird functional diversity and ecosystem services in tropical forests, agroforests and agricultural areas. J Ornithol 153:S153–S161CrossRefGoogle Scholar
  53. Şekercioğlu CH, Ehrlich PR, Daily GC, Aygen D, Goehring D, Sandi R (2002) Disappearance of insectivorous birds from tropical forest fragments. Proc Natl Acad Sci USA 99:263–267CrossRefPubMedPubMedCentralGoogle Scholar
  54. Şekercioğlu CH, Loarie SR, Brenes FO, Ehrlich PR, Daily GC (2007) Persistence of forest birds in the Costa Rican agricultural countryside. Conserv Biol 21:482–494CrossRefPubMedGoogle Scholar
  55. Shanahan M, So S, Compton SG, Corlett R (2001) Fig-eating by vertebrate frugivores: a global review. Biol Rev Camb Philos Soc 76:529–572CrossRefPubMedGoogle Scholar
  56. Shrivastava RJ, Heinen J (2007) A microsite analysis of resource use around Kaziranga National Park, India. J Environ Dev 16:207–226CrossRefGoogle Scholar
  57. Stouffer PC, Bierregaard RO Jr (1995) Use of Amazonian forest fragments by understory insectivorous birds. Ecology 76:2429–2445CrossRefGoogle Scholar
  58. Terborgh J (1986) Keystone plant resources in the tropical forest. In: Soulé ME (ed) Conservation biology, the science of scarcity and diversity. Sinauer, Sunderland, pp 330–344Google Scholar
  59. Tscharntke T, Şekercioğlu CH, Dietsch TV, Sodhi NS, Hoehn P, Tylianakis JM (2008) Landscape constraints on functional diversity of birds and insects in tropical agroecosystems. Ecology 89:944–951CrossRefPubMedGoogle Scholar
  60. Van Bael SA, Philpott SM, Greenberg R, Bichier P, Barber NA, Mooney KA, Gruner DS (2008) Birds as predators in tropical agroforestry systems. Ecology 89:928–934CrossRefPubMedGoogle Scholar
  61. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New YorkCrossRefGoogle Scholar
  62. Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Thomas J. Matthews
    • 1
    • 2
    Email author
  • H. Eden W. Cottee-Jones
    • 3
  • Tom P. Bregman
    • 4
    • 5
  • Robert J. Whittaker
    • 3
    • 6
  1. 1.GEES (School of Geography Earth and Environmental Sciences)The University of BirminghamBirminghamUK
  2. 2.CE3C – Centre for Ecology, Evolution and Environmental Changes/Azorean Biodiversity Group and Univ. dos Açores –Depto de Ciências AgráriasAngra do HeroísmoPortugal
  3. 3.Biodiversity Research Group, School of Geography and the Environment, Oxford University Centre for the EnvironmentUniversity of OxfordOxfordUK
  4. 4.Edward Grey Institute, Department of ZoologyUniversity of OxfordOxfordUK
  5. 5.Global Canopy ProgrammeOxfordUK
  6. 6.Center for Macroecology, Evolution and Climate, Natural History Museum of DenmarkUniversity of CopenhagenCopenhagenDenmark

Personalised recommendations