Abstract
Recent concern over increasing loss of biodiversity has prompted considerable interest in the role of urban green spaces as reservoirs of local biodiversity. This study assessed the diversity of three indicator taxa - plants, ants and birds - on golf courses spanning a wide range of environmental variation in terms of climate, elevation, course age, size and connectivity to native woodland. Species richness and community composition was further compared between contrasting on-course habitat types that reflect different management intensities. We identified a set of taxon-specific environmental correlates indicating an intricate interplay of landscape- and local-scale variables that affect local species diversity. Our results show that floristic diversity is positively associated with the amount of rainfall, whereas ant and bird diversity are related to local-scale factors, particularly the number of trees and the size of water features on a site. The amount of on-course native habitat was a strong predictor of plant and ant diversity and was also associated with the number of unique species at the site level; this reinforces the value of remnant habitat patches as local biodiversity reservoirs that represent mini hot-spots in an otherwise species-poor urban landscape. Community composition for all three taxa differed markedly between non-playing and playing areas, with boundary and remnant habitats generally having more diverse, species-rich communities. Our results suggest that local floral and faunal biodiversity on urban golf courses can be enhanced by creating woody non-playing areas and, especially, by preserving, restoring or expanding remnant habitats.
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References
Andersen AN (1986) Diversity, seasonality and community organization of ants at adjacent heath and woodland sites in Southeastern Australia. Aust J Zool 34:53–64. https://doi.org/10.1071/zo9860053
Andersen AN (1991) The ants of Southern Australia: A guide to the Bassian fauna. CSIRO, Melbourne
Andersen AN (1995) A classification of Australian ant communities, based on functional groups which parallel plant life-forms in relation to stress and disturbance. J Biogeogr 22:15–29. https://doi.org/10.2307/2846070
Andersen AN, Hoffmann BD, Muller WJ, Griffiths AD (2002) Using ants as bioindicators in land management: simplifying assessment of ant community responses. J Appl Ecol 39:8–17. https://doi.org/10.1046/j.1365-2664.2002.00704.x
Andersen AN, Majer JD (2004) Ants show the way down under: invertebrates as bioindicators in land management. Front Ecol Environ 2:291–298. https://doi.org/10.1890/1540-9295(2004)002[0292:ASTWDU]2.0.CO;2
Andersson E, Barthel S, Borgström S, Colding J, Elmqvist T, Folke C, Gren Å (2014) Reconnecting cities to the biosphere: stewardship of green infrastructure and urban ecosystem services. AMBIO 43(4):445–453
Aronson MF, La Sorte FA, Nilon CH, Katti M, Goddard MA, Lepczyk CA, Warren PS, Williams NS, Cilliers S, Clarkson B, Dobbs C, Dolan R, Hedblom M, Klotz S, Kooijmans JL, Kuhn I, Macgregor-Fors I, McDonnell M, Mortberg U, Pysek P, Siebert S, Sushinsky J, Werner P, Winter M (2014) A global analysis of the impacts of urbanization on bird and plant diversity reveals key anthropogenic drivers. Proc R Soc B 281:20133330. https://doi.org/10.1098/rspb.2013.3330
Bailey S (2007) Increasing connectivity in fragmented landscapes: an investigation of evidence for biodiversity gain in woodlands. For Ecol Manag 238:7–23. https://doi.org/10.1016/j.foreco.2006.09.049
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
Blair RB (1999) Birds and butterflies along an urban gradient: surrogate taxa for assessing biodiversity? Ecol Appl 9:164–170. https://doi.org/10.1890/1051-0761(1999)009[0164:BABAAU]2.0.CO;2
Brudvig LA, Damschen EI, Tewksbury JJ, Haddad NM, Levey DJ (2009) Landscape connectivity promotes plant biodiversity spillover into non-target habitats. Proc Natl Acad Sci U S A 106:9328–9332. https://doi.org/10.1073/pnas.0809658106
Chapin FS III, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, Hooper DU, Lavorel S, Sala OE, Hobbie SE, Mack MC, Díaz S (2000) Consequences of changing biodiversity. Nature 405:234–242. https://doi.org/10.1038/35012241
Colding J, Folke C (2009) The role of golf courses in biodiversity conservation and ecosystem management. Ecosystems 12:191–206. https://doi.org/10.1007/s10021-008-9217-1
Collinge SK (1996) Ecological consequences of habitat fragmentation: implications for landscape architecture and planning. Landsc Urban Plan 36:59–77. https://doi.org/10.1016/S0169-2046(96)00341-6
Colwell RK (2013) EstimateS: Statistical estimation of species richness and shared species from samples. Version 9.1. http://purl.oclc.org/estimates
DECCW (2009) The native vegetation of the Sydney Metropolitan Catchment Management Authority Area. Hurstville
Dunn RR, Agosti D, Andersen AN, Arnan X, Bruhl CA, Cerda X, Ellison AM, Fisher BL, Fitzpatrick MC, Gibb H, Gotelli NJ, Gove AD, Guenard B, Janda M, Kaspari M, Laurent EJ, Lessard JP, Longino JT, Majer JD, Menke SB, McGlynn TP, Parr CL, Philpott SM, Pfeiffer M, Retana J, Suarez AV, Vasconcelos HL, Weiser MD, Sanders NJ (2009) Climatic drivers of hemispheric asymmetry in global patterns of ant species richness. Ecol Lett 12:324–333. https://doi.org/10.1111/j.1461-0248.2009.01291.x
Doick KJ, Peace A, Hutchings TR (2014) The role of one large greenspace in mitigating London’s nocturnal urban heat island. Sci Total Environ 493:662–671. https://doi.org/10.1016/j.scitotenv.2014.06.048
Gadsdon SR, Dagley JR, Wolsley PA, Power SA (2010) Relationships between lichen community composition and concentrations of NO2 and NH3. Environ Pollut 158:2553–2560. https://doi.org/10.1016/j.envpol.2010.05.019
Gange AC, Lindsay DE, Schofield JM (2003) The ecology of golf courses. Biologist 50:63–68
Garden JG, McAlpine CA, Possingham HP, Jones DN (2007) Habitat structure is more important than vegetation composition for local-level management of native terrestrial reptile and small mammal species living in urban remnants: a case study from Brisbane, Australia. Austral Ecol 32:669–685. https://doi.org/10.1111/j.1442-9993.2007.01750.x
Gaston KJ (1996) Biodiversity. A biology of numbers and differences. Blackwell Science, London
Gaston KJ, Blackburn TM (2000) Pattern and process in macroecology. Blackwell Science, Oxford
Gregory RD, Gibbons DW, Donald PF (2002) Bird census and survey techniques. In: Sutherland WJ, Newton I, Green RE (eds) Bird ecology and conservation. A Handbook of Techniques. Oxford University Press, New York
Grimm NB, Faeth SH, Golubiewski NE, Redman CL, Wu J, Bai X, Briggs JM (2008) Global change and the ecology of cities. Science 319(5864):756–760
Hagen M, Kissling WD, Rasmussen C, De Aguiar MAM, Brown LE, Carstensen DW, Alves-Dos-Santos I, Dupont YL, Edwards FK, Genini J, Guimarães PR, Jenkins GB, Jordano P, Kaiser-Bunbury CN, Ledger ME, Maia KP, Marquitti FMD, McLaughlin T, Morellato LPC, O'Gorman EJ, Trøjelsgaard K, Tylianakis JM, Vidal MM, Woodward G, Olesen JM (2012) Biodiversity, species interactions and ecological networks in a fragmented world. Adv Ecol Res 46:89–210. https://doi.org/10.1016/B978-0-12-396992-7.00002-2
Hartig T, Mitchell R, De Vries S, Frumkin H (2014) Nature and health. Annu Rev Public Health 35:207–228. https://doi.org/10.1146/annurev-publhealth-032013-182443
Hartig T, Kahn PH Jr (2016) Living in cities, naturally. Science 352:938–940. https://doi.org/10.1126/science.aaf3759
Hodgkison SC, Hero JM, Warnken J (2007a) The conservation value of suburban golf courses in a rapidly urbanising region of Australia. Landsc Urban Plan 79:323–337. https://doi.org/10.1016/j.landurbplan.2006.03.009
Hodgkison SC, Hero JM, Warnken J (2007b) The efficacy of small-scale conservation efforts, as assessed on Australian golf courses. Biol Conserv 135:592–602. https://doi.org/10.1016/j.biocon.2006.11.001
Hudson M-AR, Bird DM (2009) Recommendations for design and management of golf courses and green spaces based on surveys of breeding bird communities in Montreal. Landsc Urban Plan 92:335–346. https://doi.org/10.1016/j.landurbplan.2009.05.017
Hui FKC, Taskinen S, Pledger S, Foster SD, Warton DI, O'Hara RB (2015) Model-based approaches to unconstrained ordination. Methods Ecol Evol 6:399–411. https://doi.org/10.1111/2041-210x.12236
Hui FKC (2016) Boral - Bayesian ordination and regression analysis of multivariate abundance data in R. Methods Ecol Evol 7:744–750. https://doi.org/10.1111/2041-210X.12514
Kong F, Yin H, Nakagoshi N, Zong Y (2010) Urban green space network development for biodiversity conservation: identification based on graph theory and gravity modeling. Landsc Urban Plan 95:16–27. https://doi.org/10.1016/j.landurbplan.2009.11.001
Kreft H, Jetz W (2007) Global patterns and determinants of vascular plant diversity. Proc Natl Acad Sci USA 104:5925–5930. https://doi.org/10.1073/pnas.0608361104
Lassau SA, Hochuli DF (2004) Effects of habitat complexity on ant assemblages. Ecography 27:157–164. https://doi.org/10.1111/j.0906-7590.2004.03675.x
Lee MA, Power SA (2013) Direct and indirect effects of roads and road vehicles on the plant community composition of calcareous grasslands. Environ Pollut 176:106–113. https://doi.org/10.1016/j.envpol.2013.01.018
Lin BB, Fuller RA (2013) FORUM: Sharing or sparing? How should we grow the world’s cities? J Appl Ecol 50:1161–1168. https://doi.org/10.1111/1365-2664.12118
Lindborg R, Eriksson O (2004) Historical landscape connectivity affects present plant species diversity. Ecology 85:1840–1845. https://doi.org/10.1890/04-0367
Lopez R, Potter DA (2003) Biodiversity of ants (Hymenoptera: Formicidae) in golf course and lawn turf habitats in Kentucky. Sociobiology 42:701–713
MacArthur RH, Wilson EO (1967) The theory of island biogeography. Princeton University Press, Princeton
MacNally R (2000) Regression and model-building in conservation biology, biogeography and ecology: the distinction between – and reconciliation of – ‘predictive’ and ‘explanatory’ models. Biodivers Conserv 9:655–671. https://doi.org/10.1023/A:100898592
Magurran AE (2004) Measuring biological diversity. Blackwell, Oxford
Maron M, Grey MJ, Catterall CP, Major RE, Oliver DL, Clarke MF, Loyn RH, Mac Nally R, Davidson I, Thomson JR, Andersen A (2013) Avifaunal disarray due to a single despotic species. Divers Distrib 19:1468–1479. https://doi.org/10.1111/ddi.12128
Mata L, Threlfall CG, Williams NSG, Hahs AK, Malipatil M, Stork NE, Livesley SJ (2017) Conserving herbivorous and predatory insects in urban green spaces. Sci Rep 7:40970. https://doi.org/10.1038/srep40970
McKinnley ML (2002) Urbanisation, biodiversity & conservation. Bioscience 52:883–890. https://doi.org/10.1641/0006-3568(2002)052[0883:UBAC]2.0.CO;2
O’Brien RM (2007) A caution regarding rules of thumb for variance inflation factors. Qual Quant 41:673–690. https://doi.org/10.1007/s11135-006-9018-6
Oliver TH, Smithers RJ, Bailey S, Walmsley CA, Watts K (2012) A decision framework for considering climate change adaptation in biodiversity conservation planning. J Appl Ecol 49:1247–1255. https://doi.org/10.1111/1365-2664.12003
Ossola A, Nash MA, Christie FJ, Hahs AK, Livesley SJ (2015) Urban habitat complexity affects species richness but not environmental filtering of morphologically-diverse ants. PeerJ 3:e1356. https://doi.org/10.7717/peerj.1356
Pardini R, de Bueno AA, Gardner TA, Prado PI, Metzger JP (2010) Beyond the fragmentation threshold hypothesis: regime shifts in biodiversity across fragmented landscapes. PLoS One 5:e13666. https://doi.org/10.1371/journal.pone.0013666
R Development CoreTeam (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3–900051–07-0, URL http://www.R-project.org/. R version 3.2.0
Rice B, Westoby M (1983) Plant species richness at the 0.1 hectare scale in Australian vegetation compared to other continents. Vegetatio 52:129–140
Rottenborn SC (1999) Predicting the impacts of urbanization on riparian bird communities. Biol Conserv 88:289–299. https://doi.org/10.1016/S0006-3207(98)00128-1
Saarikivi J, Idström L, Venn S, Niemelä J, Kotze DJ (2010) Carabid beetle assemblages associated with urban golf courses in the greater Helsinki area. Eur J Entomol 107:553–561. https://doi.org/10.14411/eje.2010.064
Sala OE, Chapin FS III, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774. https://doi.org/10.1126/science.287.5459.1770
Shanahan DF, Miller C, Possingham HP, Fuller RA (2011) The influence of patch area and connectivity on avian communities in urban revegetation. Biol Conserv 144:722–729. https://doi.org/10.1016/j.biocon.2010.10.014
Shannon CE (1948) A mathematical theory of communication. Bell Syst Tech J 27:379–423. https://doi.org/10.1002/j.1538-7305.1948.tb01338.x
Shattuck SO (1999) Australian ants: their biology and ddentification. CSIRO, Collingwood
Sorace A, Visentin M (2007) Avian diversity on golf courses and surrounding landscapes in Italy. Landsc Urban Plan 81:81–90. https://doi.org/10.1016/j.landurbplan.2006.10.014
Southwood TRE, Brown VK, Reader PM (1983) Continuity of vegetation in space and time: a comparison of insects' habitat templet in different successional stages. Res Popul Ecol 25(3 Suppl):61–74. https://doi.org/10.1007/BF02539630
Tanner RA, Gange AC (2005) Effects of golf courses on local biodiversity. Landsc Urban Plan 71:137–146. https://doi.org/10.1016/j.landurbplan.2004.02.004
Terman MR (1997) Natural links: naturalistic golf courses as wildlife habitat. Landsc Urban Plan 38:183–197. https://doi.org/10.1016/S0169-2046(97)00033-9
Threlfall CG, Walker K, Williams NSG, Hahs AK, Mata L, Stork N, Livesley SJ (2015) The conservation value of urban green space habitats for Australian native bee communities. Biol Conserv 187:240–248. https://doi.org/10.1016/j.biocon.2015.05.003
Threlfall CG, Williams NSG, Hahs AK, Livesley SJ (2016) Approaches to urban vegetation management and the impacts on urban bird and bat assemblages. Landsc Urban Plan 153:28–39. https://doi.org/10.1016/j.landurbplan.2016.04.011
Threlfall CG, Mata L, Mackie JA, Hahs AK, Stork NE, Williams NSG, Livesley SJ (2017) Increasing biodiversity in urban green spaces through simple vegetation interventions. J Appl Ecol. https://doi.org/10.1111/1365-2664.12876
Tozer M (2003) The native vegetation of the Cumberland Plain, Western Sydney: systematic classification and field identification of communities. Cunninghamia 8:1–75
Turrini T, Knop E (2015) A landscape ecology approach identifies important drivers of urban biodiversity. Glob Chang Biol 21:1652–1667. https://doi.org/10.1111/gcb.12825
Underwood EC, Fisher BL (2006) The role of ants in conservation monitoring: if, when, and how. Biol Conserv 132:166–182. https://doi.org/10.1016/j.biocon.2006.03.022
Venables WN, Ripley BD (2002) Modern applied statistics with S, 4th edn. Springer, New York ISBN 0-387-95457-0
Vidrih B, Medved S (2013) Multiparametric model of urban park cooling island. Urban For Urban Green 12:220–229. https://doi.org/10.1016/j.ufug.2013.01.002
Wang Y, Naumann U, Wright S, Warton D (2015) mvabund: statistical methods for analysing multivariate abundance data. R package version 3.10.4. http:// CRAN.R-project.org/package=mvabund
Yasuda M, Koike F (2006) Do golf courses provide a refuge for flora and fauna in Japanese urban landscapes? Landsc Urban Plan 75:58–68. https://doi.org/10.1016/j.landurbplan.2004.12.004
Yasuda M, Koike F, Terman M (2008) How management practices affect arthropod communities on Japanese golf courses? Landsc Ecol Eng 4:133–138. https://doi.org/10.1007/s11355-008-0048-1
Yates M, Andrew NR (2011) Comparison of ant community composition across different land-use types: assessing morphological traits with more common methods. Aust Entomol 50(2):118–124. https://doi.org/10.1111/j.1440-6055.2010.00795.x
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effect models and extensions in R. Springer, New York
Acknowledgements
We wish to thank the Greater Sydney Local Land Services who provided the funding for the study. We are grateful to Prof Alan Andersen at CSIRO in Darwin for his generous assistance in ant species identification. We are also grateful for the generous help provided by Dr. Alison Downing and Karen Marais in identifying plant specimens at the Herbarium at Macquarie University. We would like to thank Golf NSW, and the general managers and superintendents of all the involved golf courses for participating in the study.
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Nooten, S.S., Schultheiss, P., Wright, J. et al. What shapes plant and animal diversity on urban golf courses?. Urban Ecosyst 21, 565–576 (2018). https://doi.org/10.1007/s11252-017-0728-4
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DOI: https://doi.org/10.1007/s11252-017-0728-4