Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-19T08:43:08.250Z Has data issue: false hasContentIssue false

Effects of habitat fragmentation on the bats of Kakamega Forest, western Kenya

Published online by Cambridge University Press:  14 August 2019

Paul W. Webala*
Affiliation:
Maasai Mara University, Department of Forestry and Wildlife Management, P.O. Box 861, Narok 20500, Kenya
Jeremiah Mwaura
Affiliation:
Karatina University, School of Natural Resources and Environmental Studies, P.O. Box 1957, Karatina 10101, Kenya
Joseph M. Mware
Affiliation:
Karatina University, School of Natural Resources and Environmental Studies, P.O. Box 1957, Karatina 10101, Kenya
George G. Ndiritu
Affiliation:
Karatina University, School of Natural Resources and Environmental Studies, P.O. Box 1957, Karatina 10101, Kenya
Bruce D. Patterson
Affiliation:
Integrative Research Center, Field Museum of Natural History, Chicago, IL 60605, USA
*
*Author for correspondence: Paul W. Webala, Email: [email protected]

Abstract

Habitat loss and fragmentation are major threats to biodiversity worldwide, and little is known about their effects on bats in Africa. We investigated effects of forest fragmentation on bat assemblages at Kakamega Forest, western Kenya, examining captures at edge and interior locations in three forest fragments (Buyangu, 3950 ha; Kisere, 400 ha; and Malava, 100 ha) varying in forest area and human-use regimes. Basal area, canopy cover, tree density and intensity of human use were used as predictors of bat abundance and species richness. A total of 3456 mist-net hours and 3168 harp-trap hours resulted in the capture of 4983 bats representing 26 species, eight families and four foraging ensembles (frugivores, forest-interior insectivores, forest-edge insectivores and open-space insectivores). Frugivores were frequently captured at the edges of the larger, better-protected forests, but also in the interior of the smaller, more open fragment. Forest-interior insectivores and narrow-space foragers predominated in the interiors of larger fragments but avoided the smallest one. Forest specialists showed positive associations with forest variables (canopy cover, basal area and tree density), whereas frugivores responded positively to the human-use indicators. On these bases, specialist species appear to be especially vulnerable to forest fragmentation.

Type
Research Article
Copyright
© Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature cited

Aldridge, HDJN and Rautenbach, IL (1987) Morphology, echolocation and resource partitioning in insectivorous bats. Journal of Animal Ecology 56, 763778.CrossRefGoogle Scholar
Andrén, H (1994) Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suitable habitat: a review. Oikos 71, 355366.CrossRefGoogle Scholar
Anthony, ELP (1988) Age determination in bats. Pp. 4758 in Kunz, TH (ed.), Ecological and Behavioral Methods for the Study of Bats. Washington, DC: Smithsonian Institution Press.Google Scholar
Barlow, J, Gardner, TA, Araujo, IS, Ávila-Pires, TC, Bonaldo, AB, Costa, JE, Esposito, MC, Ferreira, LV, Hawes, J, Hernandez, MIM, Hoogmoed, MS, Leite, RN, Lo-Man-Hung, NF, Malcolm, JR, Martins, MBL, Mestre, AM, Miranda-Santos, R, Nunes-Gutjahr, AL, Overal, WL, Parry, L, Peters, SL, Ribeiro-Junior, MA, Da Silva, MNF, Da Silva Motta, C and Peres, CA (2007) Quantifying the biodiversity value of tropical primary, secondary, and plantation forests. Proceedings of the National Academy of Sciences USA 104, 1855518560.CrossRefGoogle ScholarPubMed
Barlow, J, Lennox, GD, Ferreira, J, Berenguer, E, Lees, AC, Nally, RM, Thomson, JR, Ferraz, SFDB, Louzada, J, Oliveira, VHF, Parry, L, Ribeiro De Castro Solar, R, Vieira, ICG, Aragào, LEOC, Begotti, RA, Braga, RF, Cardoso, TM, De Oliveira, RC Jr, Souza, CM Jr, Moura, NG, Nunes, SS, Siqueira, JV, Pardini, R, Silveira, JM, Vaz-De-Mello, FZ, Veiga, RCS, Venturieri, A and Gardner, TA (2016) Anthropogenic disturbance in tropical forests can double biodiversity loss from deforestation. Nature 535, 144147.CrossRefGoogle ScholarPubMed
Clarke, KR and Gorley, RN (2001) PRIMER v5: User Manual/Tutorial. Plymouth: PRIMER-E, 91 pp.Google Scholar
Cosson, JF, Pons, JM and Masson, D (1999) Effects of forest fragmentation on frugivorous and nectarivorous bats in French Guiana. Journal of Tropical Ecology 15, 515534.CrossRefGoogle Scholar
Cunto, GC and Bernard, E (2012) Neotropical bats as indicators of environmental disturbance: what is the emerging message? Acta Chiropterologica 14, 143151.CrossRefGoogle Scholar
Day, RW and Quinn, GP (1989) Comparisons of treatments after an analysis of variance in ecology. Ecological Monographs 59, 433463.CrossRefGoogle Scholar
Denzinger, A and Schnitzler, H-U (2013) Bat guilds, a concept to classify the highly diverse foraging and echolocation behaviors of microchiropteran bats. Frontiers in Physiology 4, 164. 10.3389/fphys.2013.00164.CrossRefGoogle ScholarPubMed
Estrada-Villegas, S, Meyer, CFJ and Kalko, EKV (2010) Effects of tropical forest fragmentation on aerial insectivorous bats in a land-bridge island system. Biological Conservation 143, 597608.CrossRefGoogle Scholar
Ewers, RM and Didham, RK (2006) Confounding factors in the detection of species responses to habitat fragmentation. Biological Reviews 81, 117142.CrossRefGoogle ScholarPubMed
Fahrig, L (2003) Effects of habitat fragmentation on biodiversity. Annual Review of Ecology and Systematics 34, 487515.CrossRefGoogle Scholar
Faria, D (2006) Phyllostomid bats of a fragmented landscape in the north-eastern Atlantic forest, Brazil. Journal of Tropical Ecology 22, 531542.CrossRefGoogle Scholar
Farneda, FZ, Rocha, R, López-Baucells, A, Groenenberg, M, Silva, I, Palmeirim, JM, Bobrowiec, PED and Meyer, CFJ (2015) Trait-related responses to habitat fragmentation in Amazonian bats. Journal of Applied Ecology 52, 13811391.CrossRefGoogle Scholar
Fenton, MB (1997) Science and the conservation of bats. Journal of Mammalogy 78, 114.CrossRefGoogle Scholar
García-García, JL, Santos-Moreno, A and Kraker-Castañeda, C (2014) Ecological traits of phyllostomid bats associated with sensitivity to tropical forest fragmentation in Los Chimalpas, Mexico. Tropical Conservation Science 7, 457474.CrossRefGoogle Scholar
Glenday, J (2006) Carbon storage and emissions offset potential in an East African tropical rainforest. Forest Ecology and Management 235, 7283.CrossRefGoogle Scholar
Gorresen, PM and Willig, MR (2004) Landscape responses of bats to habitat fragmentation in Atlantic forest of Paraguay. Journal of Mammalogy 85, 688697.CrossRefGoogle Scholar
Grindal, SD and Brigham, RM (1998) Effects of small-scale habitat fragmentation on activity by insectivorous bats. Journal of Wildlife Management 62, 9961003.CrossRefGoogle Scholar
Guthiga, P, Mburu, J and Holm-Mueller, K (2008) Factors influencing local communities’ satisfaction levels with different forest management approaches of Kakamega Forest, Kenya. Environmental Management 41, 696706.CrossRefGoogle ScholarPubMed
Handley, CO Jr, Wilson, DE and Gardner, AL (1991) Demography and natural history of the common fruit bat, Artibeus jamaicensis, on Barro Colorado Island, Panama. Smithsonian Contributions to Zoology 511, 1173.CrossRefGoogle Scholar
Hansen, MC, Potapov, PV, Moore, R, Hancher, M, Turubanova, S, Tyukavina, A, Thau, D, Stehman, S, Goetz, S and Loveland, T (2013) High-resolution global maps of 21st-century forest cover change. Science 342, 850853.CrossRefGoogle ScholarPubMed
Harper, KA, MacDonald, SE, Burton, PJ, Chen, J, Brosofke, KD, Saunders, SC, Euskirchen, ES, Roberts, D, Jaiteh, MS and Esseen, PA (2005) Edge influence on forest structure and composition in fragmented landscapes. Conservation Biology 19, 115.CrossRefGoogle Scholar
Henry, M, Cosson, JF and Pons, JM (2010) Modelling multi-scale spatial variation in species richness from abundance data in a complex Neotropical bat assemblage. Ecological Modelling 221, 20182027.CrossRefGoogle Scholar
Hill, JK and Hamer, KC (2004) Determining impacts of habitat modification on diversity of tropical forest fauna: the importance of spatial scale. Journal of Applied Ecology 41, 744754.CrossRefGoogle Scholar
Jones, KE, Purvis, A and Gittleman, JL (2003) Biological correlates of extinction risk in bats. American Naturalist 161, 601614.CrossRefGoogle ScholarPubMed
Jones, G, Jacobs, DS, Kunz, TH, Willig, MR and Racey, PA (2009) Carpe noctem: the importance of bats as bioindicators. Endangered Species Research 8, 93115.CrossRefGoogle Scholar
Kingston, T, Francis, CM, Zubaid, A and Kunz, TH (2003) Species richness in an insectivorous bat assemblage from Malaysia. Journal of Tropical Ecology 19, 6779.CrossRefGoogle Scholar
Klingbeil, BT and Willig, MR (2009) Guild-specific responses of bats to landscape composition and configuration in fragmented Amazonian rainforest. Journal of Applied Ecology 46, 203213.CrossRefGoogle Scholar
Klingbeil, BT and Willig, MR (2010) Seasonal differences in population-, ensemble- and community-level responses of bats to landscape structure in Amazonia. Oikos 119, 16541664.CrossRefGoogle Scholar
Kokwaro, JO (1988) Conservation status of the Kakamega Forest in Kenya: the easternmost relic of the equatorial rain forests of Africa. Monographs in Systematic Botany of the Missouri Botanical Garden 25, 471489.Google Scholar
Kunz, TH and Lumsden, LF (2003) Ecology of cavity and foliage roosting bats. In Kunz, TH and Fenton, MB (eds), Bat Ecology. Chicago, IL: University of Chicago Press, pp. 390.Google Scholar
Kunz, TH and Pierson, ED (1994) Bats of the world: an introduction. In Nowak, RM (ed.), Walker’s Bats of the World. Baltimore, MD: Johns Hopkins University Press, pp. 146.Google Scholar
Lagan, P, Mannan, S and Matsubayashi, H (2007) Sustainable use of tropical forests by reduced-impact logging in Deramakot Forest Reserve, Sabah, Malaysia. Ecological Research 22, 414421.CrossRefGoogle Scholar
Lane, DJW, Kingston, T and Lee, BPY-H (2006) Dramatic decline in bat species richness in Singapore, with implications for Southeast Asia. Biological Conservation 131, 584593.CrossRefGoogle Scholar
Laurance, WF, Laurance, SG, Ferreira, LV, Rankin-De Merona, JM, Gascon, C and Lovejoy, TE (1997) Biomass collapse in Amazonian forest fragments. Science 278, 11171118.CrossRefGoogle Scholar
Laurance, WF, Perez-Salicrup, D, Delamonica, P, Fearnside, PM, D’Angelo, S, Jerozolinski, A, Pohl, L and Lovejoy, TE (2001) Rain forest fragmentation and the structure of Amazonian liana communities. Ecology 82, 105116.CrossRefGoogle Scholar
Laurance, WF, Nascimento, H, Laurance, SG, Andrade, A, Ribeiro, J, Giraldo, JP, Lovejoy, TE, Condit, R, Chave, J and D’Angelo, S (2006) Rapid decay of tree community composition in Amazonian forest fragments. Proceedings of the National Academy of Sciences USA 103, 1901019014.CrossRefGoogle ScholarPubMed
Laurance, WF, Camargo, JL, Luizão, RC, Laurance, SG, Pimm, SL, Bruna, EM, Stouffer, PC, Williamson, GB, Benítez-Malvido, J and Vasconcelos, HL (2011) The fate of Amazonian forest fragments: a 32-year investigation. Biological Conservation 144, 5667.CrossRefGoogle Scholar
Lepš, J and Šmilauer, P (2003) Multivariate Analysis of Ecological Data using CANOCO. Czech Republic: University of South Bohemia and Cambridge: Cambridge University Press.CrossRefGoogle Scholar
MacSwiney, MC, Clarke, FM and Racey, PA (2008) What you see is not what you get: the role of ultrasonic detectors in increasing inventory completeness in Neotropical bat assemblages. Journal of Applied Ecology 45, 13641371.CrossRefGoogle Scholar
Magurran, AE (2004) Measuring Biological Diversity. Oxford: Blackwell Publishing. 256 pp.Google Scholar
Marinello, MM and Bernard, E (2014) Wing morphology of Neotropical bats: a quantitative and qualitative analysis with implications for habitat use. Canadian Journal of Zoology 92, 141147.CrossRefGoogle Scholar
Metzger, JP and Décamps, H (1997) The structural connectivity threshold: an hypothesis in conservation biology at the landscape scale. Acta Oecologica 18, 112.CrossRefGoogle Scholar
Meyer, CFJ and Kalko, EKV (2008) Assemblage-level responses of phyllostomid bats to tropical forest fragmentation: land-bridge islands as a model system. Journal of Biogeography 35, 17111726.CrossRefGoogle Scholar
Meyer, CFJ, Fründ, J, Pineda, W and Kalko, EKV (2008) Ecological correlates of vulnerability to fragmentation in Neotropical bats. Journal of Applied Ecology 45, 381391.CrossRefGoogle Scholar
Meyer, CFJ, Aguiar, LMS, Aguirre, LF, Baumgarten, J, Clarke, FM, Cosson, J-F, Villegas, SE, Fahr, J, Faria, D, Furey, N, Henry, M, Hodgkison, R, Jenkins, RKB, Jung, KG, Kingston, T, Kunz, TH, Gonzalez, MCM, Moya, I, Patterson, BD, Pons, J-M, Racey, PA, Rex, K, Sampaio, EM, Solari, S, Stoner, KE, Voigt, CC, Staden, DV, Weise, CD and Kalko, EKV (2011) Accounting for detectability improves estimates of species richness in tropical bat surveys. Journal of Applied Ecology 48, 777787.CrossRefGoogle Scholar
Meyer, CFJ, Aguiar, LMS, Aguirre, LF, Baumgarten, J, Clarke, FM, Cosson, J-F, Estrada-Villegas, S, Fahr, J, Faria, D, Furey, N, Henry, M, Jenkins, RKB, Kunz, TH, MacSwiney Gonzalez, MC, Moya, I, Pons, J-M, Racey, PA, Rex, K, Sampaio, EM, Stoner, KE, Voigt, CC, Von Staden, D, Weise, CD and Kalko, EKV (2015) Species undersampling in tropical bat surveys: effects on emerging biodiversity patterns. Journal of Animal Ecology 84, 113123.CrossRefGoogle ScholarPubMed
Meyer, CFJ, Struebig, M and Willig, MR (2016) Responses of tropical bats to habitat fragmentation, logging, and deforestation. In Voigt, CC and Kingston, T (eds), Bats in the Anthropocene: Conservation of Bats in a Changing World. Heidelberg: Springer, pp. 63103.CrossRefGoogle Scholar
Mitchell, N, Schaab, G and Wägele, W (2009) Kakamega Forest ecosystem: an introduction to the natural history and the human context. BIOTA East Africa Report 5. Karlsruher Geowisseschaftliche Schriften A 17, 156. Karlsruhe: Karlsruhe University of Applied Sciences, Faculty of Geomatics.Google Scholar
Montiel, S, Estrada, A and Leon, P (2006) Bat assemblages in a naturally fragmented ecosystem in the Yucatan Peninsula, Mexico: species richness, diversity and spatio-temporal dynamics. Journal of Tropical Ecology 22, 267276.CrossRefGoogle Scholar
Morris, RJ (2010) Anthropogenic impacts on tropical forest biodiversity: a network structure and ecosystem functioning perspective. Philosophical Transactions of the Royal Society B: Biological Sciences 365, 37093718.CrossRefGoogle ScholarPubMed
Mueller-Dombois, D and Ellenberg, H (1974) Aims and Methods of Vegetation Ecology. New York, NY: John Wiley and Sons. 547 pp.Google Scholar
Müller, D and Mburu, J (2009) Forecasting hotspots of forest clearing in Kakamega Forest, Western Kenya. Forest Ecology and Management 257, 968977.CrossRefGoogle Scholar
Neuweiler, G (1984) Foraging, echolocation and audition in bats. Naturwissenschaften 71, 446455.CrossRefGoogle Scholar
Norberg, UM and Rayner, JMV (1987) Ecological morphology and flight in bats (Mammalia; Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philosophical Transactions of the Royal Society of London Series B Biological Sciences 316, 335427.CrossRefGoogle Scholar
O’Farrell, M and Gannon, W (1999) A comparison of acoustic versus capture techniques for the inventory of bats. Journal of Mammalogy 80, 2430.CrossRefGoogle Scholar
Pardini, R, Faria, D, Accacio, GM, Laps, RR, Mariano, E, Paciencia, MLB, Dixo, M and Baumgarten, J (2009) The challenge of maintaining Atlantic forest biodiversity: a multi-taxa conservation assessment of specialist and generalist species in an agro-forestry mosaic in southern Bahia. Biological Conservation 142, 11781190.CrossRefGoogle Scholar
Patterson, BD and Webala, PW (2012) Keys to the bats (Mammalia: Chiroptera) of East Africa. Fieldiana: Life and Earth Sciences 6, 163.Google Scholar
Pielou, EC (1975) Ecological Diversity. New York, NY: Wiley InterScience. 165 pp.Google Scholar
Presley, SJ, Willig, MR, Wunderle, JM and Saldanha, LN (2008) Effects of reduced-impact logging and forest physiognomy on bat populations of lowland Amazonian forest. Journal of Applied Ecology 45, 1425.CrossRefGoogle Scholar
Rocha, R, López-Baucells, A, Farneda, FZ, Groenenberg, M, Bobrowiec, PED, Cabeza, M, Palmeirim, JM and Meyer, CFJ (2016) Consequences of a large-scale fragmentation experiment for Neotropical bats: disentangling the relative importance of local and landscape-scale effects. Landscape Ecology 32, 3145.CrossRefGoogle Scholar
Safi, K and Kerth, G (2004) A comparative analysis of specialization and extinction risk in temperate-zone bats. Conservation Biology 18, 12931303.CrossRefGoogle Scholar
Saldana-Vázquez, RA and Munguía-Rosas, MA (2013) Lunar phobia in bats and its ecological correlates: a meta-analysis. Mammalian Biology 78, 216219.CrossRefGoogle Scholar
Schnitzler, H-U and Kalko, KMV (2001) Echolocation by insect-eating bats. BioScience 51, 557569.CrossRefGoogle Scholar
Schnitzler, HU, Moss, CF and Denzinger, A (2003) From spatial orientation to food acquisition in echolocating bats. Trends in Ecology and Evolution 18, 386394.CrossRefGoogle Scholar
Sherwin, HA, Montgomery, WI and Lundy, MG (2013) The impact and implications of climate change for bats. Mammal Review 43, 171182.CrossRefGoogle Scholar
Simpson, EH (1949) Measurement of diversity. Nature 163, 688.CrossRefGoogle Scholar
Sokal, RR and Rohlf, FJ (1995) Biometry: The Principles and Practice of Statistics in Biological Research, Third edition. New York, NY: W.H. Freeman. 887 pp.Google Scholar
Struebig, MJ, Kingston, T, Zubaid, A, Adnan, AM, Nichols, RA and Rossiter, SJ (2008) Conservation value of forest fragments to Palaeotropical bats. Biological Conservation 141, 21122126.CrossRefGoogle Scholar
Struebig, MJ, Kingston, T, Zubaid, A, Lecomber, SC, Adnan, A, Turner, A, Kelly, J, Bozek, MS and Rossiter, SJ (2009) Conservation importance of limestone karst outcrops to Palaeotropical bats in a fragmented landscape. Biological Conservation 142, 20892096.CrossRefGoogle Scholar
Struebig, MJ, Kingston, T, Petit, EJ, Le Comber, SC, Zubaid, A, Mohd-Adnan, A and Rossiter, SJ (2011) Parallel declines in species and genetic diversity in tropical forest fragments. Ecology Letters 14, 582590.CrossRefGoogle ScholarPubMed
Thies, W, Kalko, EKV and Schnitzler, H (1998) The roles of echolocation and olfaction in two Neotropical fruit-eating bats, Carollia perspicillata and C. castanea, feeding on Piper. Behavioral Ecology and Sociobiology 42, 397409.CrossRefGoogle Scholar
Wagner, P, Kohler, J, Schmitz, A and Bohme, W (2008) The biogeographical assignment of a west Kenyan rain forest remnant: further evidence from analysis of its reptile fauna. Journal of Biogeography 35, 13491361.CrossRefGoogle Scholar
Watling, JI and Donnelly, MA (2006) Fragments as islands: a synthesis of faunal responses to habitat patchiness. Conservation Biology 20, 10161025.CrossRefGoogle ScholarPubMed
Webala, PW, Rydell, J, Dick, CW, Musila, S and Patterson, BD (2019) Echolocation calls of some high duty-cycle bats from Kenya. Journal of Bat Research and Conservation 12, 1020.Google Scholar
World Bank (2008) World Development Indicators 2008. Washington, DC: World Bank.Google Scholar