Abstract
Cemeteries can help conserve biodiversity in urban landscapes, but their capacity to support native species is likely to be influenced by variables at different spatial scales. There is growing evidence on how landscape and patch-level attributes influence biodiversity in urban parks. However, there is limited evidence about cemeteries. Park cemeteries are dominated by vegetation because they are managed to simulate traditional parks, and thus, could contribute to the conservation of native fauna in cities. We present the first study on how patch variables (cemetery size and vegetation density) and landscape variables (vegetation cover and road density within 1 km) influence the richness and abundance of native birds in urban park cemeteries. During summer and autumn, we surveyed birds in park cemeteries in the Mediterranean city of Santiago, Chile – a large Latin American city located in a biodiversity hotspot. We recorded 42 bird species (38 native and 4 exotic). We found that cemeteries surrounded by high vegetation cover supported more native birds, whereas cemeteries surrounded by high road density supported low native bird abundance. We also found a seasonal effect: cemeteries supported more individuals of native birds in autumn than in summer, probably due to birds migrating to our study area from higher latitude, altitude, and surrounding environments, in their search for milder weather conditions. Our findings demonstrate that park cemeteries host a variety of native birds, which contributes to maintain biodiversity in urban landscapes. However, the surrounding landscape influences their capacity to support native birds and to conserve biodiversity in cities.
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References
Aronson MF, Lepczyk CA, Evans KL et al (2017) Biodiversity in the city: key challenges for urban green space management. Front Ecol Environ 15:189–196. https://doi.org/10.1002/fee.1480
Baillie J, Griffiths J, Turvey S, Loh J, Collen B (2010) Evolution lost: status and trends of the world’s vertebrates. Zoological Society of London, London
Bar-Massada A, Radeloff VC, Stewart SI (2014) Biotic and abiotic effects of human settlement in the wildland-urban interface. Bioscience 64:429–437. https://doi.org/10.1093/biosci/biu039
Barrett GW, Barrett TL (2001) Cemeteries as repositories of natural and cultural diversity. Conserv Biol 15:1820–1824. https://doi.org/10.1046/j.1523-1739.2001.00410.x
Barton K (2013) MuMIn: Multi-model inference. R package version 1.15.6. http://CRAN.R-project.org/package=MuMIn
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Beninde J, Veith M, Hochkirch A (2015) Biodiversity in cities needs space: a meta-analysis of factors determining intra-urban biodiversity variation. Ecol Lett 18:581–592. https://doi.org/10.1111/ele.12427
Bino G, Levin N, Darawshi S, Van Der Hal N, Reich-Solomon A, Kark S (2008) Accurate prediction of bird species richness patterns in an urban environment using Landsat-derived NDVI and spectral unmixing. Int J Remote Sens 29:3675–3700. https://doi.org/10.1080/01431160701772534
Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135. https://doi.org/10.1016/j.tree.2008.10.008
Botzat A, Fischer LK, Kowarik I (2016) Unexploited opportunities in understanding liveable and biodiverse cities. A review on urban biodiversity perception and valuation. Glob Environ Chang 39:220–233. https://doi.org/10.1016/j.gloenvcha.2016.04.008
Čanády A, Mošanský L (2017) Public cemetery as a biodiversity hotspot for birds and mammals in the urban environment of Kosice city (Slovakia). Zool Ecol 27:185–195. https://doi.org/10.1080/21658005.2017.1366024
Canedoli C, Manenti R, Padoa-Schioppa E (2018) Birds biodiversity in urban and periurban forests: environmental determinants at local and landscape scales. Urban Ecosyst. https://doi.org/10.1007/s11252-018-0757-7
Censo (2017) Primera entrega de resultados definitivos Censo 2017: Cantidad de personas por sexo y edad. http://www.censo2017.cl/descargue-aqui-resultados-de-comunas/. Accessed 25 Apr 2018
Chace JF, Walsh JJ (2006) Urban effects on native avifauna: a review. Landsc Urban Plan 74:46–69. https://doi.org/10.1016/j.landurbplan.2004.08.007
Evans KL, Greenwood JJD, Gaston KJ (2005) Dissecting the species–energy relationship. Proc R Soc B Biol Sci 272:2155–2163. https://doi.org/10.1098/rspb.2005.3209
Fischer LK, Rodorff V, von der Lippe M, Kowarik I (2016) Drivers of biodiversity patterns in parks of a growing south American megacity. Urban Ecosyst 19:1231–1249. https://doi.org/10.1007/s11252-016-0537-1
Fuda RK, Ryan SJ, Cohen JB, Hartter J, Frair JL (2016) Assessing impacts to primary productivity at the park edge in Murchison falls conservation area, Uganda. Ecosphere 7:e01486. https://doi.org/10.1002/ecs2.1486
Gagne SA, Fahrig L (2010) The trade-off between housing density and sprawl area: Minimising impacts to forest breeding birds. Basic Appl Ecol 11:723–733. https://doi.org/10.1016/j.baae.2010.09.001
Hernández HJ, Villaseñor NR (2018) Twelve-year change in tree diversity and spatial segregation in the Mediterranean city of Santiago, Chile. Urban For Urban Green 29:10–18. https://doi.org/10.1016/j.ufug.2017.10.017
Ikin K, Beaty RM, Lindenmayer DB, Knight E, Fischer J, Manning AD (2013) Pocket parks in a compact city: how do birds respond to increasing residential density? Landsc Ecol 28:45–56. https://doi.org/10.1007/s10980-012-9811-7
Ikin K, Le Roux DS, Rayner L et al (2015) Key lessons for achieving biodiversity-sensitive cities and towns. Ecol Manag Restor 16:206–214. https://doi.org/10.1111/emr.12180
INE (2015) Medio Ambiente, informe anual. Período de información: 2009 – 2013. Instituto Nacional de Estadística, Santiago
Jaganmohan M, Vailshery LS, Mundoli S, Nagendra H (2018) Biodiversity in sacred urban spaces of Bengaluru, India. Urban For Urban Green 32:64–70. https://doi.org/10.1016/j.ufug.2018.03.021
Jokimaki J, Suhonen J (1993) Effects of urbanization on the breeding bird species richness in Finland: a biogeographical comparison. Ornis Fenn 70:71–77
Kociolek AV, Clevenger AP, St. Clair CC, Proppe DS (2011) Effects of road networks on bird populations. Conserv Biol 25:241–249. https://doi.org/10.1111/j.1523-1739.2010.01635.x
Kowarik I, Buchholz S, von der Lippe M, Seitz B (2016) Biodiversity functions of urban cemeteries: evidence from one of the largest Jewish cemeteries in Europe. Urban For Urban Green 19:68–78. https://doi.org/10.1016/j.ufug.2016.06.023
Lim HC, Sodhi NS (2004) Responses of avian guilds to urbanisation in a tropical city. Landsc Urban Plan 66:199–215. https://doi.org/10.1016/s0169-2046(03)00111-7
Magle SB, Hunt VM, Vernon M, Crooks KR (2012) Urban wildlife research: past, present, and future. Biol Conserv 155:23–32. https://doi.org/10.1016/j.biocon.2012.06.018
Marzluff JM (2017) A decadal review of urban ornithology and a prospectus for the future. Ibis 159:1–13. https://doi.org/10.1111/ibi.12430
McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127:247–260. https://doi.org/10.1016/j.biocon.2005.09.005
Ministerio del Medio Ambiente (2014) Quinto Informe Nacional de Biodiversidad de Chile ante el Convenio sobre la Diversidad Biológica (CBD). Ministerio del Medio Ambiente, Santiago
Morelli F, Mikula P, Benedetti Y, Bussière R, Jerzak L, Tryjanowski P (2018) Escape behaviour of birds in urban parks and cemeteries across Europe: evidence of behavioural adaptation to human activity. Sci Total Environ 631-632:803–810. https://doi.org/10.1016/j.scitotenv.2018.03.118
Muñoz-Sáez A, Perez-Quezada JF, Estades CF (2017) Agricultural landscapes as habitat for birds in Central Chile. Rev Chil Hist Nat 90. https://doi.org/10.1186/s40693-017-0067-0
Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. https://doi.org/10.1038/35002501
Myneni RB, Hall FG, Sellers PJ, Marshak AL (1995) Interpretation of spectral vegetation indexes. IEEE Trans Geosci Remote Sens 33:481–486. https://doi.org/10.1109/36.377948
Ockendon N, Davis SE, Miyar T, Toms MP (2009) Urbanization and time of arrival of common birds at garden feeding stations. Bird Stud 56:405–410. https://doi.org/10.1080/00063650902937313
Pettorelli N, Vik JO, Mysterud A, Gaillard J-M, Tucker CJ, Stenseth NC (2005) Using the satellite-derived NDVI to assess ecological responses to environmental change. Trends Ecol Evol 20:503–510. https://doi.org/10.1016/j.tree.2005.05.011
Post W, Cruz A, McNair DB (1993) The north American invasion pattern of the shiny cowbird. J Field Ornithol 64:32–41
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing Vienna, Austria. https://www.R-project.org/
Raftery AE (1995) Bayesian model selection in social research. Sociol Methodol 25:111–163. https://doi.org/10.2307/271063
Seto KC, Guneralp B, Hutyra LR (2012) Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. P Natl Acad Sci USA 109:16083–16088. https://doi.org/10.1073/pnas.1211658109
Smallbone LT, Luck GW, Wassens S (2011) Anuran species in urban landscapes: relationships with biophysical, built environment and socio-economic factors. Landsc Urban Plan 101:43–51. https://doi.org/10.1016/j.landurbplan.2011.01.002
Sol D, Bartomeus I, González-Lagos C, Pavoine S (2017) Urbanisation and the loss of phylogenetic diversity in birds. Ecol Lett 20:721–729. https://doi.org/10.1111/ele.12769
Tryjanowski P, Morelli F, Mikula P et al (2017) Bird diversity in urban green space: a large-scale analysis of differences between parks and cemeteries in Central Europe. Urban For Urban Green 27:264–271. https://doi.org/10.1016/j.ufug.2017.08.014
United Nations (2018) 2018 revision of the world urbanization prospects. Department of Economic and Social Affairs. Population Division, New York
Villaseñor NR, Driscoll DA, Gibbons P, Calhoun AJK, Lindenmayer DB (2017a) The relative importance of aquatic and terrestrial variables for frogs in an urbanizing landscape: key insights for sustainable urban development. Landsc Urban Plan 157:26–35. https://doi.org/10.1016/j.landurbplan.2016.06.006
Villaseñor NR, Tulloch AIT, Driscoll DA, Gibbons P, Lindenmayer DB (2017b) Compact development minimizes the impacts of urban growth on native mammals. J Appl Ecol 54:794–804. https://doi.org/10.1111/1365-2664.12800
Weier J, Herring D (2000) Measuring vegetation (NDVI & EVI). NASA. Available: https://earthobservatory.nasa.gov/Features/MeasuringVegetation/. Accessed March 2018
Acknowledgments
We thank park cemeteries for granting access to sites; Jecar Rodríguez, Catalina Muñoz, Javiera Benito, Joaquín Foncea, Manuel Villalobos and Matías Carrasco for their assistance during data collection; and Trevor Walter and Franco Magni for proof-reading and commenting on previous versions of the manuscript. Authors thank funding from CONICYT FONDECYT Postdoctorado No. 3170179: Conservation in the city (Comisión Nacional de Investigación Científica y Tecnológica, CONICYT, Chile) granted to NRV.
Funding
NRV was supported by project CONICYT - FONDECYT No. 3170179: Conservation in the city (Comisión Nacional de Investigación Científica y Tecnológica, CONICYT, Chile).
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Villaseñor, N.R., Escobar, M.A.H. Cemeteries and biodiversity conservation in cities: how do landscape and patch-level attributes influence bird diversity in urban park cemeteries?. Urban Ecosyst 22, 1037–1046 (2019). https://doi.org/10.1007/s11252-019-00877-3
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DOI: https://doi.org/10.1007/s11252-019-00877-3