Journal Home > Volume 10 , Issue 1
Background

Although the species-urban green area relationship (SARu) has been analyzed worldwide, the global consistency of its parameters, such as the fit and the slope of models, remains unexplored. Moreover, the SARu can be explained by 20 different models. Therefore, our objective was to evaluate which models provide a better explanation of SARus and, focusing on the power model, to evaluate the global heterogeneity in its fit and slope.

Methods

We tested the performance of multiple statistical models in accounting for the way in which species richness increases with area, and examined whether variability in model form was associated with various methodological and environmental factors. Focusing on the power model, we analyzed the global heterogeneity in the fit and slope of the models through a meta-analysis.

Results

Among 20 analyzed models, the linear model provided the best fit to the most datasets, was the top ranked model according to our efficiency criterion, and was the top overall ranked model. The Kobayashi and power models were the second and third overall ranked models, respectively. The number of green areas and the minimum number of species within a green area were the only significant variables explaining the variation in model form and performance, accounting for less than 10% of the variation. Based on the power model, there was a consistent overall fit (r2 = 0.50) and positive slope of 0.20 for the species richness increase with area worldwide.

Conclusions

The good fit of the linear model to our SARu datasets contrasts with the non-linear SAR frequently found in true and non-urban habitat island systems; however, this finding may be a result of the small sample size of many SARu datasets. The overall power model slope of 0.20 suggests low levels of isolation among urban green patches, or alternatively that habitat specialist and area sensitive species have already been extirpated from urban green areas.


menu
Abstract
Full text
Outline
About this article

A global consistent positive effect of urban green area size on bird richness

Show Author's information Lucas M. Leveau1 ( )Adriana Ruggiero2Thomas J. Matthews3,4M. Isabel Bellocq1,^
Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires-IEGEBA (CONICET-UBA), Intendente Güiraldes 2160, Ciudad Universitaria, Pab 2, Piso 4, C1428EGA Buenos Aires, Argentina
Laboratorio Ecotono, Centro Regional Universitario Bariloche-Universidad Nacional del Comahue, INIBIOMA-CONICET, 8400 San Carlos de Bariloche, Río Negro, Argentina
GEES (School of Geography, Earth and Environmental Sciences) and the Birmingham Institute of Forest Research, The University of Birmingham, Birmingham B15 2TT, UK
Departamento de Ciências e Engenharia do Ambiente, CE3C-Centre for Ecology, Evolution and Environmental Changes/Azorean Biodiversity Group and Universidade dos Açores, 9700-042 Angra do Heroísmo, Açores, Portugal

M. Isabel Bellocq—Deceased on 9 July 2019

Abstract

Background

Although the species-urban green area relationship (SARu) has been analyzed worldwide, the global consistency of its parameters, such as the fit and the slope of models, remains unexplored. Moreover, the SARu can be explained by 20 different models. Therefore, our objective was to evaluate which models provide a better explanation of SARus and, focusing on the power model, to evaluate the global heterogeneity in its fit and slope.

Methods

We tested the performance of multiple statistical models in accounting for the way in which species richness increases with area, and examined whether variability in model form was associated with various methodological and environmental factors. Focusing on the power model, we analyzed the global heterogeneity in the fit and slope of the models through a meta-analysis.

Results

Among 20 analyzed models, the linear model provided the best fit to the most datasets, was the top ranked model according to our efficiency criterion, and was the top overall ranked model. The Kobayashi and power models were the second and third overall ranked models, respectively. The number of green areas and the minimum number of species within a green area were the only significant variables explaining the variation in model form and performance, accounting for less than 10% of the variation. Based on the power model, there was a consistent overall fit (r2 = 0.50) and positive slope of 0.20 for the species richness increase with area worldwide.

Conclusions

The good fit of the linear model to our SARu datasets contrasts with the non-linear SAR frequently found in true and non-urban habitat island systems; however, this finding may be a result of the small sample size of many SARu datasets. The overall power model slope of 0.20 suggests low levels of isolation among urban green patches, or alternatively that habitat specialist and area sensitive species have already been extirpated from urban green areas.

Keywords: Birds, Urbanization, Urban parks, Conservation macroecology, Habitat islands, Species-area relationships, Species-urban green area relationship

References(94)

Anderson MJ, Willis TJ. Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology. 2003;84:511-25.

Batllori X, Uribe F. Aves nidificantes de los jardines de Barcelona. Misc Zool. 1998;12:283-93.

Beninde J, Veith M, Hochkirch A. Biodiversity in cities needs space: a meta-analysis of factors determining intra-urban biodiversity variation. Ecol Lett. 2015;18:581-92.

Bino G, Levin N, Darawshi S, Van Der Hal N, Reich-Solomon A, Kark S. Accurate prediction of bird species richness patterns in an urban environment using Landsat-derived NDVI and spectral unmixing. Int J Remote Sens. 2008;29:3675-700.

Blair RB. Land use and avian species diversity along an urban gradient. Ecol Appl. 1996;6:506-19.

Borenstein MH, Higgins LV, Rothstein JPT. Introduction to meta-analysis. Chichester: Wiley; 2009.

DOI

Burghardt KT, Tallamy DW, Gregory Shriver W. Impact of native plants on bird and butterfly biodiversity in suburban landscapes. Conserv Biol. 2009;23:219-24.

Burnham KP, Anderson DR. Model selection and multimodel inference: a practical information-theoretic approach. New York: Springer Science & Business Media; 2002.

Chace JF, Walsh JJ. Urban effects on native avifauna: a review. Landsc Urban Plan. 2006;74:46-69.

Chavez-Almonacid CA. Relación entre la avifauna, la vegetación y las construcciones en plazas y parques de la ciudad de Valdivia. Tesis de licenciatura: Universidad Austral de Chile, Valdivia; 2014.

Chivian E, Bernstein AS. Embedded in nature: human health and biodiversity. Environ Health Perspect. 2004;112:A12.

Connor EF, McCoy ED. The statistics and biology of the species-area relationship. Am Nat. 1979;113:791-833.

Croci S, Butet A, Georges A, Aguejdad R, Clergeau P. Small urban woodlands as biodiversity conservation hot-spot: a multi-taxon approach. Landsc Ecol. 2008;23:1171-86.

De la Peña M. Nidos de aves argentinas. Santa Fe: Universidad Nacional del Litoral; 2010.
Del Hoyo J, Elliott A, Christie D (1994-2011) Handbook of the birds of the world. Barcelona: Lynx editions

Dengler J. Which function describes the species-area relationship best? A review and empirical evaluation. J Biogeogr. 2009;36:728-44.

Drakare S, Lennon JJ, Hillebrand H. The imprint of the geographical, evolutionary and ecological context on species-area relationships. Ecol Lett. 2006;9:215-27.

Dunn RR, Gavin MC, Sanchez MC, Solomon JN. The pigeon paradox: dependence of global conservation on urban nature. Conserv Biol. 2006;20:1814-6.

Evans BS, Reitsma R, Hurlbert AH, Marra PP. Environmental filtering of avian communities along a rural-to-urban gradient in Greater Washington, DC, USA. Ecosphere. 2018;9:2402.

Faeth SH, Bang C, Saari S. Urban biodiversity: patterns and mechanisms. Ann NY Acad Sci. 2011;1223:69-81.

Faggi A, Perepelizin P. Riqueza de aves a lo largo de un gradiente de urbanización en la ciudad de Buenos Aires. Revista del Museo Argentino de Ciencias Naturales nueva serie. 2006;8:289-97.

Fattorini S, Mantoni C, De Simoni L, Galassi D. Island biogeography of insect conservation in urban green spaces. Environ Conserv. 2018a;45:1-10.

Fattorini S, Lin G, Mantoni C. Avian species-area relationships indicate that towns are not different from natural areas. Environ Conserv. 2018b;45:419-24.

Fernández-Juricic E. Avian spatial segregation at edges and interiors of urban parks in Madrid, Spain. Biodivers Conserv. 2001;10:1303-16.

Fernández-Juricic E, Jokimäki J. A habitat island approach to conserving birds in urban landscapes: case studies from southern and northern Europe. Biodivers Conserv. 2001;10:2023-43.

Fuller RA, Irvine KN, Devine-Wright P, Warren PH, Gaston KJ. Psychological benefits of greenspace increase with biodiversity. Biol Lett. 2007;3:390-4.

Garaffa PI, Filloy J, Bellocq MI. Bird community responses along urban-rural gradients: does town size matter? Landsc Urban Plan. 2009;90:33-41.

Garden J, Mcalpine C, Peterson ANN, Jones D, Possingham H. Review of the ecology of Australian urban fauna: a focus on spatially explicit processes. Austral Ecol. 2006;31:126-48.

Grimm NB, Faeth SH, Golubiewski NE, Redman CL, Wu J, Bai X, Briggs JM. Global change and the ecology of cities. Science. 2008;319:756-60.

Gurevitch J, Hedges LV. Statistical issues in ecological meta-analyses. Ecology. 1999;80:1142-9.

Guilhaumon F, Mouillot D, Gimenez O. mmSAR: an R-package for multimodel species-area relationship inference. Ecography. 2010;33:420-4.

Hanski I, Zurita GA, Bellocq MI, Rybicki J. The species-fragmented area relationship. P Natl Acad Sci USA. 2013;110:12715-20.

He F, Legendre P. On species-area relations. Am Nat. 1995;148:719-37.

Hedges L, Olkin I. Statistical models for meta-analysis. New York: Academic Press; 1985.

Hilty SL. Birds of Venezuela. New Jersey: Princeton University Press; 2002.

Hilty SL, Brown WL, Brown B. A guide to the birds of Colombia. New Jersey: Princeton University Press; 1986.

Hopewell S, McDonald S, Clarke M, Egger M. Grey literature in meta-analyses of randomized trials of health care interventions. Cochrane Database Syst Rev. 2007. https://doi.org/10.1002/14651858.MR000010.pub3.

Hubbell SP. The unified neutral theory of biodiversity and biogeography. California: Princeton University Press; 2001.

Hume R. Complete birds of Britain and Europe. London: Dorling Kindersley; 2002.

Husté A, Boulinier T. Determinants of bird community composition on patches in the suburbs of Paris, France. Biol Conserv. 2011;144:243-52.

Jokimäki J, Huhta E. Artificial nest predation and abundance of birds along an urban gradient. Condor. 2000;102:838-47.

Kazmierczak K, van Perlo B. A field guide to the birds of India, Sri Lanka, Pakistan, Nepal, Bhutan, Bangladesh, and the Maldives. New Delhi: Om Book Service; 2000.

La Sorte FA, Lepczyk CA, Aronson MF, Goddard MA, Hedblom M, Katti M, MacGregor-Fors I, Mörtberg U, Nilon CH, Warren PS, Williams NS. The phylogenetic and functional diversity of regional breeding bird assemblages is reduced and constricted through urbanization. Divers Distrib. 2018;24:928-38.

Leveau LM, Leveau CM. Does urbanization affect the seasonal dynamics of bird communities in urban parks? Urban Ecosyst. 2016;19:631-47.

Lizée MH, Mauffrey JF, Tatoni T, Deschamps-Cottin M. Monitoring urban environments on the basis of biological traits. Ecol Indicat. 2011;11:353-361.

MacArthur RH, Wilson EO. The theory of island biogeography. Monographs in Population Biology, vol. 1. New Jersey: Princeton University Press; 1967.

MacGregor-Fors I, Ortega-Álvarez R. Fading from the forest: bird community shifts related to urban park site-specific and landscape traits. Urban For Urban Green. 2011;10:239-46.

MacGregor-Fors I, Morales-Pérez L, Schondube JE. Migrating to the city: responses of neotropical migrant bird communities to urbanization. Condor. 2010;112:711-7.

Magle SB, Hunt VM, Vernon M, Crooks KR. Urban wildlife research: past, present, and future. Biol Conserv. 2012;155:23-32.

Matthews TJ. Analysing and modelling the impact of habitat fragmentation on species diversity: a macroecological perspective. Front Biogeogr. 2015;7:60-8.

Matthews TJ, Guilhaumon F, Triantis KA, Borregaard MK, Whittaker RJ. On the form of species-area relationships in habitat islands and true islands. Global Ecol Biogeogr. 2016a;25:847-58.

Matthews TJ, Triantis KA, Rigal F, Borregaard MK, Guilhaumon F, Whittaker RJ. Island species-area relationships and species accumulation curves are not equivalent: an analysis of habitat island datasets. Global Ecol Biogeogr. 2016b;25:607-18.

Matthews TJ, Triantis K, Whittaker RJ, Guilhaumon F. sars: an R package for fitting, evaluating and comparing species-area relationship models. Ecography. 2019;42:1446-55.

McKinney ML. Urbanization as a major cause of biotic homogenization. Biol Conserv. 2006;127:247-60.

Miller JR. Hobbs RJ Conservation where people live and work. Conserv Biol. 2002;16:330-7.

Mitchell MH. Observations on birds of southeastern Brazil. Toronto: University of Toronto Press; 1957.

Møller AP, Diaz M, Flensted-Jensen E, Grim T, Ibáñez-Álamo JD, Jokimäki J, Mänd R, Markó G, Tryjanowski P. High urban population density of birds reflects their timing of urbanization. Oecologia. 2012;170:867-75.

Munyenyembe F, Harris J, Hone J, Nix H. Determinants of bird populations in an urban area. Aust J Ecol. 1989;14:549-57.

Murgui E. Effects of seasonality on the species-area relationship: a case study with birds in urban parks. Global Ecol Biogeogr. 2007;16:319-29.

National Geographic Society (US). Field guide to the birds of North America. New York: National Geographic Society; 1999.

Natuhara Y, Imai C. Prediction of species richness of breeding birds by landscape-level factors of urban woods in Osaka Prefecture, Japan. Biodivers Conserv. 1999;8:239-53.

Nielsen AB, van den Bosch M, Maruthaveeran S, van den Bosch CK. Species richness in urban parks and its drivers: a review of empirical evidence. Urban Ecosyst. 2014;17:305-27.

Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND, Powell GVN, Underwood EC, D'amico JA, Itoua I, Strand HE, Morrison JC, Loucks CJ, Allnutt TF, Ricketts TH, Kura Y, Lamoreux JF, Wettengel WW, Hedao P, Kassem KR. Terrestrial ecoregions of the world: a new map of life on earth. Bioscience. 2001;51:933-8.

Ortega-Álvarez R, MacGregor-Fors I. Dusting-off the file: a review of knowledge on urban ornithology in Latin America. Landsc Urban Plan. 2011;101:1-10.

Paradis E, Baillie SR, Sutherland WJ, Gregory RD. Patterns of natal and breeding dispersal in birds. J Anim Ecol. 1998;67:518-36.

Park CR, Lee WS. Relationship between species composition and area in breeding birds of urban woods in Seoul, Korea. Landsc Urban Plan. 2000;51:29-36.

Pautasso M, Böhning-Gaese K, Clergeau P, et al. Global macroecology of bird assemblages in urbanized and semi-natural ecosystems. Global Ecol Biogeogr. 2011;20:426-36.

Peterson R, Mountfort G, Hollom PAD, Díaz G. Guía de campo de las aves de España y demás países de Europa. Barcelona: Omega; 1973.

Preston FW. The canonical distribution of commonness and rarity: part Ⅰ. Ecology. 1962;43:185-215.

Rahbek C. The relationship among area, elevation, and regional species richness in neotropical birds. Am Nat. 1997;149:875-902.

R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, 2019. http://www.R-project.org/.

Rosenberg MS. The file-drawer problem revisited: a general weighted method for calculating fail-safe numbers in meta-analysis. Evolution. 2005;59:464-8.

Rosenberg MS, Adams DC, Gurevitch J. MetaWin: statistical software for meta-analysis. Sunderland: Sinauer Associates; 2000.

Rosenthal R. The file drawer problem and tolerance for null results. Psychol Bull. 1979;86:638.

Rosenzweig ML. Species diversity in space and time. Cambridge: Cambridge University Press; 1985.

Scheiner SM, Chiarucci A, Fox GA, Helmus MR, McGlinn DJ, Willig MR. The underpinnings of the relationship of species richness with space and time. Ecol Monogr. 2011;81:195-213.

Seto KC, Fragkias M, Güneralp B, Reilly MK. A meta-analysis of global urban land expansion. PLoS ONE. 2011;6:e23777.

Shochat E, Warren PS, Faeth SH, McIntyre NE, Hope D. From patterns to emerging processes in mechanistic urban ecology. Trends Ecol Evol. 2006;21:186-91.

Stott I, Soga M, Inger R, Gaston KJ. Land sparing is crucial for urban ecosystem services. Front Ecol Environ. 2015;13:387-93.

Szlavecz K, Warren P, Pickett S. Biodiversity on the urban landscape. In: Concotta RP, Gorenflo LJ, editors. Human populations, its influences on biological diversity. Ecological studies, vol. 214. Berlin: Springer-Verlag; 2011.https://doi.org/10.1007/978-3-642-16707-2_6
DOI
Sukhdev P. Foreword. In: Elmqvist T, Fragkias M, Goodness J, Güneralp B, Marcotullio PJ, McDonald RI, Parnell S, Schewenius M, Sendstad M, Seto KC, Wilkinson C, editors. Urbanization, biodiversity and ecosystems services: Challenges and opportunities. Dordrecht: Springer; 2013.

Sutherland GD, Harestad AS, Price K, Lertzman KP. Scaling of natal dispersal distances in terrestrial birds and mammals. Conserv ecol. 2000. https://doi.org/10.5751/ES-00184-040116.

Tjørve E. Shapes and functions of species-area curves: a review of possible models. J Biogeogr. 2003;30:827-35.

Tjørve E. Shapes and functions of species-area curves (Ⅱ): a review of new models and parameterizations. J Biogeogr. 2009;36:1435-45.

Tjørve E, Turner WR. The importance of samples and isolates for species-area relationships. Ecography. 2009;32:391-400.

Triantis KA, Guilhaumon F, Whittaker RJ. The island species-area relationship: biology and statistics. J Biogeogr. 2012;39:215-31.

Tummers B. Data Thief Ⅲ (v. 1.1). 2006. http://www.datathief.org/. Accessed 25 Mar 2017.
United Nations. World urbanization prospects: the 2014 revision. Highlights (ST/ESA/SER.A/352). 2014.

Urquiza A, Mella JE. Riqueza y diversidad de aves en parques de Santiago durante el período estival. Boletín Chileno de Ornitología. 2002;9:12-21.

Vaccaro AS, Filloy J, Bellocq MI. What land use better preserves taxonomic and functional diversity of birds in a grassland biome? Avian Conserv Ecol. 2019;14:1.

Watling JI, Donnelly MA. Fragments as islands: a synthesis of faunal responses to habitat patchiness. Conserv Biol. 2006;20:1016-25.

Wild Bird Society of Japan. A field guide to the birds of Japan. Tokyo: Kodansha International Limited; 1982.
Yamashina Y. Birds in Japan: a field guide. Tokyo: Tokyo news Limited; 1961. p. 1961.

Zhou D, Chu LM. How would size, age, human disturbance, and vegetation structure affect bird communities of urban parks in different seasons? J Ornithol. 2012;153:1101-12.

Publication history
Copyright
Acknowledgements
Rights and permissions

Publication history

Received: 26 February 2019
Accepted: 24 July 2019
Published: 21 August 2019
Issue date: January 2019

Copyright

© The Author(s) 2019.

Acknowledgements

Acknowledgements

We greatly appreciate the help with QGis software provided by Carolina Ramos. LML thanks the support of Lucia Gonzalez Salinas. We are very thankful to Carolina Berget, Andrés Seijas, Karen Ikin, Michael O'Neal Campbell and Pilar Carbó-Ramírez, who generously gave data for the analysis. The comments of Simone Fattorini and three anonymous reviewers greatly improved earlier versions of the manuscript. The research was funded by the Consejo Nacional de Investigaciones Científicas y Técnicas and the Universidad de Buenos Aires (Argentina). The authors dedicate this piece of work to our co-author M.I. Bellocq, dearest colleague and friend who will always be in our hearts and memories.

Rights and permissions

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Return