Abstract
Tropical forests are increasingly threatened by anthropogenic activities often resulting in habitat and biodiversity loss. To effectively manage and protect these areas, it is important to have an understanding of the factors affecting their biodiversity. Previous research has shown that birds in tropical regions are severely affected by human-induced habitat conversion and disturbance. The effects, however, are often area and guild-specific and the underlying mechanisms are frequently unclear. In this study, we disentangle and quantify the direct and indirect effects of human population density, distance to forest edge, habitat disturbance, and vegetation structure and composition on the total abundance and species richness of birds in Kakamega Forest, Kenya. Specifically, we use structural equation modeling to develop and test path models, which reflect the potential causal relationships between the bird assemblages and the chosen explanatory factors. Relationships were tested on the overall bird community and on five different guilds, classified according to birds’ forest specialization and feeding preferences (i.e. forest specialists, generalists and visitors, and frugivores and insectivores). Results showed that habitat disturbance, caused by logging, had a weak positive direct effect on the bird communities, but also had a strong detrimental indirect effect, particularly on the total abundance and species richness of forests specialists and insectivores. The negative effect was mediated through changes in the forest’s vegetation structure and composition. Shorter distances to the forest edge also had a negative effect, on all bird categories except on forest visitors, which also benefited from higher levels of disturbance. Our study shows that although in some cases habitat disturbance may have no strong direct negative effects it can still negatively influence bird communities in an indirect way. In the case of Kakamega Forest, we suggest that to conserve bird communities it is important to maintain the forest’s compositional and structural diversity by reducing human-induced habitat disturbance, such as illegal logging activities.
Similar content being viewed by others
References
Althof AJ (2005) Human impact on flora and vegetation of Kakamega forest, Kenya: structure, distribution and disturbance of plant communities in an East African rainforest. PhD Thesis, Universität Koblenz-Landau, Germany
Bennun L, Dranzoa C, Pomeroy D (1996) The forest birds of Kenya and Uganda. J East Afr Nat Hist 85(1):23–48
Bennun L, Njoroge P (2000) Important bird areas in Kenya. Ostrich 71(1–2):164–167
Bibby C, Burgess N, Hill D (1992) Bird census techniques. British trust for ornithology and the royal society for the protection of birds. Academic Press, London
Blackett H (1994) Forest Inventory Report No. 3. Kakamega Forest Department/KIFCON, Nairobi, Kenya
Bleher B, Bohning-Gaese K (2006) S04-4 the role of birds in seed dispersal and its consequences for forest ecosystems. Acta Zool Sin 52(Supplement):116–1199
Bleher B, Uster D, Bergsdorf T (2006) Assessment of threat status and management effectiveness in Kakamega forest, Kenya. Biodivers Conserv 15(4):1159–1177
Booth H, Purves DW, Newbold T, Scharlemann JP, Butchart SH, Sekercioglu ÇH, Alkemade R (2012) Ecological traits affect the response of tropical forest bird
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer Science & Business Media, New York
Cincotta RP, Wisnewski J, Engelman R (2000) Human population in the biodiversity hotspots. Nature 404(6781):990–992
Danoff-Burg J, Xu C (2006) Biodiversity calculator, http://www.columbia.edu/itc/cerc/danoff-burg/MBD_Links.html
Danson FM, Hetherington D, Morsdorf F, Koetz B, Allgower B (2007) Forest canopy gap fraction from terrestrial laser scanning. Geosci Remote Sens Lett IEEE 4(1):157–160
Dranzoa C (1998) The avifauna 23 years after logging in Kibale National Park, Uganda. Biodivers Conserv 7(6):777–797
Eshiamwata GW, Berens DG, Bleher B, Dean WRJ, Böhning-Gaese K (2006) Bird assemblages in isolated Ficus trees in Kenyan farmland. J Trop Ecol 22:723–726
Farwig N, Berens DG (2012) Imagine a world without seed dispersers: a review of threats, consequences and future directions. Basic Appl Ecol 13(2):109–115
Farwig N, Böhning-Gaese K, Bleher B (2006) Enhanced seed dispersal of Prunus africana in fragmented and disturbed forests? Oecologia 147(2):238–252
Farwig N, Sajita N, Böhning-Gaese K (2008) Conservation value of forest plantations for bird communities in western Kenya. For Ecol Manag 255(11):3885–3892
Farwig N, Sajita N, Böhning-Gaese K (2009) Corrigendum to conservation value of forest plantations for bird communities in western Kenya [Forest Ecol. Manag. 255 (2008) 3885–3892]. For Ecol Manag 258(7):1731–1734
Fashing PJ, Forrestel A, Scully C, Cords M (2004) Long-term tree population dynamics and their implications for the conservation of the Kakamega Forest, Kenya. Biodivers Conserv 13(4):753–771
Fashing PJ, Gathua JM (2004) Spatial variability in the vegetation structure and composition of an East African rain forest. Afr J Ecol 42(3):189–197
Frazer G, Canham C, Lertzman K (2000) Departments-technological tools-gap light analyzer (GPA), version 2.0. Bull Ecol Soc Am 81(3):191–197
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 279(1740):3106–3113
Gardner TA, Barlow J, Chazdon R, Ewers RM, Harvey CA, Peres CA, Sodhi NS (2009) Prospects for tropical forest biodiversity in a human-modified world. Ecol Lett 12(6):561–582
Gibson L, Lee TM, Koh LP, Brook BW, Gardner TA, Barlow J, Peres CA, Bradshaw CJ, Laurance WF, Lovejoy TE (2011) Primary forests are irreplaceable for sustaining tropical biodiversity. Nature 478(7369):378–381
Grace JB (2006) Structural equation modeling and natural systems. University Press, Cambridge
Grace JB (2008) Structural equation modeling for observational studies. J Wildl Manag 72(1):14–22
Hewson CM, Austin GE, Gough SJ, Fuller RJ (2011) Species-specific responses of woodland birds to stand-level habitat characteristics: the dual importance of forest structure and floristics. For Ecol Manag 261:1224–1240
Howe HF, Smallwood J (1982) Ecology of seed dispersal. Annu Rev Ecol Syst 13:201–228
Kareiva P, Watts S, McDonald R, Boucher T (2007) Domesticated nature: shaping landscapes and ecosystems for human welfare. Science 316(5833):1866–1869
Kirika JM, Farwig N, Böhning-Gaese K (2008a) Effects of local disturbance of tropical forests on frugivores and seed removal of a small-seeded afrotropical tree. Conserv Biol 22(2):318–328
Kirika JM, Bleher B, Böhning-Gaese K, Chira R, Farwig N (2008b) Fragmentation and local disturbance of forests reduce frugivore diversity and fruit removal in Ficus thonningii trees. Basic Appl Ecol 9:663–672
Kissling WD, Rahbek C, Böhning-Gaese K (2007) Food plant diversity as broad-scale determinant of avian frugivore richness. Proc R Soc B 274(1611):799–808
Kissling WD, Field R, Böhning-Gaese K (2008) Spatial patterns of woody plant and bird diversity: functional relationships or environmental effects? Glob Ecol Biogeogr 17:327–339
Kokwaro J (1988) Conservation status of the Kakamega Forest in Kenya: the easternmost relic of the equatorial rain forests of Africa. Monogr Syst Bot Mo Bot Gard 25:471–489
Lindell CA, Riffell SK, Kaiser SA, Battin AL, Smith ML, Sisk TD (2007) Edge responses of tropical and temperate birds. Wilson J Ornithol 119(2):205–220
Lung T, Schaab G (2004) Change-detection in Western Kenya: the documentation of fragmentation and disturbance for Kakamega Forest and associated forest areas by means of remotely-sensed imagery. In: Proceedings of the ISPRS XXth Congress, Istanbul, Turkey, 12–23 July 2004
Lung T, Schaab G (2006) Assessing fragmentation and disturbance of west Kenyan rainforests by means of remotely sensed time series data and landscape metrics. Afr J Ecol 44(4):491–506
Lung T, Schaab G (2010) A comparative assessment of land cover dynamics of three protected forest areas in tropical eastern Africa. Environ Monit Assess 161(1–4):531–548
Lung T, Peters MK, Farwig N, Böhning-Gaese K, Schaab G (2012) Combining long-term land cover time series and field observations for spatially explicit predictions on changes in tropical forest biodiversity. Int J Remote Sens 33(1):13–40
Lung T, Lübker T, Ngochoch JK, Schaab G (2013) Human population distribution modelling at regional level using very high resolution satellite imagery. Appl Geogr 41:36–45
Magurran AE (1998) Ecological diversity and its measurement. Princeton University Press, Princeton
Maina, G. G. 2002. Effect of forest fragmentation on bird communities in Kakamega Forest, Kenya. PhD Thesis. University of Illinois at Chicago, USA
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(10):1553–1566
Mitchell RJ (1992) Testing evolutionary and ecological hypotheses using path analysis and structural equation modelling. Funct Ecol 6:123–129
Mitchell N (2004) The exploitation and disturbance history of Kakamega Forest, Western Kenya. Biota East Africa. In Bleher B. & Dalitz H. (Eds) BIOTA Report No. 1. Bielefelder Ökologische Beiträge 20
Mitchell N, Schaab G (2008) Developing a disturbance index for five East African forests using GIS to analyse historical forest use as an important driver of current land use/cover. Afr J Ecol 46:572–584
Mulwa RK, Böhning-Gaese K, Schleuning M (2012) High bird species diversity in structurally heterogeneous farmland in Western Kenya. Biotropica 44(6):801–809
Mulwa RK, Neuschulz EL, Böhning-Gaese K, Schleuning M (2013) Seasonal fluctuations of resource abundance and avian feeding guilds across forest–farmland boundaries in tropical Africa. Oikos 122(4):524–532
Nakagawa S, Freckleton RP (2011) Model averaging, missing data and multiple imputation: a case study for behavioural ecology. Behav Ecol Sociobiol 65:103–116
Newbold T, Scharlemann JP, Butchart SH, Sekercioglu ÇH, Alkemade R, Booth H, Purves DW (2013) Ecological traits affect the response of tropical forest bird species to land-use intensity. Proc R Soc B 280(1750):1471–2954
Paradis E, Claude J, Strimmer K (2004) APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290
Pugesek BH, Tomer A, Von Eye A (eds) (2003) Structural equation modeling: applications in ecological and evolutionary biology. University Press, Cambridge
R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Rogo LM, Lwande W, Chapya A, Herren HR, Miller SE An Integrated Conservation Initiative to Conserve Kakamega Forest and its Biodiversity. In: Ganeshaiah KN, Shaanker RUA, Bawa KS (eds) Proceedings of the International Conference of Tropical Ecosystems, Bangalore, 2001. ATREE, pp 56–60
Saracco JF, Collazo JA, Groom MJ (2004) How do frugivores track resources? Insights from spatial analyses of bird foraging in a tropical forest. Oecologia 139:235–245
Schleuning M, Farwig N, Peters MK, Bergsdorf T, Bleher B, Brandl R, Dalitz H, Fischer G, Freund W, Gikungu MW (2011a) Forest fragmentation and selective logging have inconsistent effects on multiple animal-mediated ecosystem processes in a tropical forest. PLoS One 6(11):e27785
Schleuning M, Blüthgen N, Flörchinger M, Braun J, Schaefer HM, Böhning-Gaese K (2011b) Specialization and interaction strength in a tropical plant–frugivore network differ among forest strata. Ecology 92:26–36
Schumacker RE, Lomax RG (2004) A beginner’s guide to structural equation modeling. Lawrence Erlbaum Associates, Mahwah
Sekercioglu CH, Daily GC, Ehrlich PR (2004) Ecosystem consequences of bird declines. Proc Natl Acad Sci 101:18042–18047
Sekercioglu CH (2006) Increasing awareness of avian ecological function. Trends Ecol Evol 21(8):464–471
Sodhi NS, Posa MRC, Lee TM, Warkentin IG (2008) Perspectives in ornithology: effects of disturbance or loss of tropical rainforest on birds. Auk 125(3):511–519
Tscharntke T, Sekercioglu CH, Dietsch TV, Sodhi NS, Hoehn P, Tylianakis JM (2008) Landscape constraints on functional diversity of birds and insects in tropical agroecosystems. Ecology 89(4):944–951
Tsingalia MH (1990) Habitat disturbance, severity and patterns of abundance in Kakamega Forest, western Kenya. Afr J Ecol 28(3):213–226
Waltert M, Bobo KS, Sainge NM, Fermon H, Mühlenberg M (2005) From forest to farmland: habitat effects on Afrotropical forest bird diversity. Ecol Appl 15(4):1351–1366
Watson JE, Whittaker RJ, Dawson TP (2004) Habitat structure and proximity to forest edge affect the abundance and distribution of forest-dependent birds in tropical coastal forests of southeastern Madagascar. Biol Conserv 120(3):311–327
Wootton JT (1994) Predicting direct and indirect effects: an integrated approach using experiments and path analysis. Ecology 75:151–165
Acknowledgments
We are thankful to Nixon Sajita, Jackson Welesi and Joash Ogutu for their assistance in the field and to two anonymous reviewers and the associate editor for their constructive feedback. This project was mainly funded by the Research Promotion Foundation in Cyprus, with co-funding from the European Union’s Structural Funds (Protocol Number PENK/SUPPORT/0308/42). Financial support for this study was also provided by the German Federal Ministry of Education and Research as part of the BIOTA Africa project (Grant numbers: 01LC0025, 01LC0405, 01LC0625) and by the research funding program “Landes-Offensive zur Entwicklung wissenschaftlich ökonomischer Exzellenz” (LOEWE) of Hesse’s Ministry of Higher Education, Research, and the Arts. TC acknowledges support of an ERC advanced grant.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Kwek Yan Chong.
Appendix
Appendix
See Table 4.
Rights and permissions
About this article
Cite this article
Mammides, C., Schleuning, M., Böhning-Gaese, K. et al. The indirect effects of habitat disturbance on the bird communities in a tropical African forest. Biodivers Conserv 24, 3083–3107 (2015). https://doi.org/10.1007/s10531-015-1001-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-015-1001-x