Vegetation attributes drive the taxonomic richness and functional composition of beetles and spiders in mountainous urban green spaces

Abstract

Urban green spaces (UGS) enhance the quality of life in urban environments and serve as habitat corridors or refuge for organisms, including beetles and spiders. The attributes of UGS allow them to harbour species that offer essential ecosystem services. However, the ability of UGS to provide services is limited by the extent to which they have been altered anthropogenically. We described the taxonomic richness and functional composition of arthropods in a mountainous urban ecosystem of Ghana by focussing on the activity of both beetles and spiders at the family level. Two main land-use types (woodlands and built-up areas) were identified and characterised based on the presence or absence of certain vegetation attributes. Sixteen plots in each land-use type with sizes 20 × 20 m were demarcated and fitted with four pitfall traps in each plot to sample continuously for eight weeks, the activity density of both beetles and spiders. Samples were sorted into families and functional groups (detritivores, fungivores, herbivores and predators). The taxonomic richness and activity density were both significantly higher in the woodlands than in the built-up areas. Similarly, all functional groups showed a higher affinity to the woodlands than the built-up areas. Habitat attributes defined by plant diversity and structural complexity were the underlying drivers explaining the differences in arthropod communities between the land-use types. Though the built-up areas seem degraded and open, the remaining small vegetation patches still support the activities of some taxa that should merit the protection of such remnant vegetation in urban ecosystems.

Keywords

Activity density / Arthropod community composition / Functional composition / Land-use change / Taxonomic richness / Mountainous urban ecosystem

References

[1] Ahrne K, Bengtsson J, Elmqvist T. Bumble bees (Bombus spp) along a gradient of increasing urbanisation. PLoS ONE, 2009, 4(5): e5574

[2] Argañaraz CI, Rubio GD, Rubio M, Castellarini F. Ground-dwelling spiders in agroecosystems of the Dry Chaco: a rapid assessment of community shifts in response to land-use changes. Biodiversity, 2020, 21(3): 125-135

[3] Bače R, Svoboda M, Vítková L (2019) Deadwood management in production forests. Management guidelines for forest managers in Central European temperate forests, (s 31). Department of Forest Ecology, Faculty of Forestry and Wood Sciences, Czech University of Life, Prague

[4] Bang C Jr Effects of urbanisation on arthropod diversity, community structure and trophic dynamics, 2010 Arizona Arizona State University

[5] Barnes AD, Scherber C, Brose U, Borer ET, Ebeling A, Gauzens B, Eisenhauer N. Biodiversity enhances the multitrophic control of arthropod herbivores. Sci Adv, 2020, 6(45): eabb6603

[6] Bergmann DJ, Brandenburg D, Petit S, Gabel M. Habitat preferences of ground beetle (Coleoptera: Carabidae) species in the northern Black Hills of South Dakota. Environ Entomol, 2012, 41(5): 1069-1076

[7] Blondel J. Guilds or functional groups: does it matter?. Oikos, 2003, 100(2): 223-231

[8] Borchard F, Buchholz S, Helbing F, Fartmann T. Carabid beetles and spiders as bioindicators for the evaluation of montane heathland restoration on former spruce forests. Biol Cons, 2014, 178: 185-192

[9] Braga RF, Korasaki V, Andresen E, Louzada J. Dung beetle community and functions along a habitat-disturbance gradient in the Amazon: a rapid assessment of ecological functions associated to biodiversity. PLoS ONE, 2013, 8(2): e57786

[10] Bray JR, Curtis JT. An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr, 1957, 27(4): 326-349

[11] Buczkowski G, Richmond DS. The effect of urbanisation on ant abundance and diversity: a temporal examination of factors affecting biodiversity. PLoS ONE, 2012, 7(8): e41729

[12] Burks JM, Philpott SM. Local and landscape drivers of parasitoid abundance, richness, and composition in urban gardens. Environ Entomol, 2017, 46(2): 201-209

[13] Cajaiba RL, Périco E, Silva WB, Santos M. Seasonal patterns in the diversity of Histerid beetles (Histeridae) are ecosystem specific? A case in Para State, Northern Brazil. Appl Ecol Environ Res, 2017, 15(4): 1227-1237

[14] Cameron RW, Brindley P, Mears M, McEwan K, Ferguson F, Sheffield D, Richardson M. Where the wild things are! Do urban green spaces with greater avian biodiversity promote more positive emotions in humans?. Urban Ecosyst, 2020, 23(2): 301-317

[15] Cardoso EJBN, Vasconcellos RLF, Bini D, Miyauchi MYH, Santos CAD, Alves PRL, Nogueira MA. Soil health: looking for suitable indicators. What should be considered to assess the effects of use and management on soil health?. Sci Agric, 2013, 70(4): 274-289

[16] Carrión-Paladines V, Fries A, Muñoz A, Castillo E, García-Ruiz R, Marín-Armijos D. Effects of land-use change on the community structure of the dung beetle (Scarabaeinae) in an altered ecosystem in Southern Ecuador. Insects, 2021, 12(4): 306

[17] Castro AV, Porrini DP, Cicchino AC (2014) Annual Activity Density of groundbeetles (Coleoptera: Carabidae) of a Celtis ehrenbergiana (Rosales: Celtidaceae) Forest of Buenos Aires Province, Argentina. J Insect Sci 14(1)

[18] Choi WI, Choi KS, Lyu DP, Lee JS, Lim J, Lee S, Park YS. Seasonal changes of functional groups in coleopteran communities in pine forests. Biodivers Conserv, 2010, 19(8): 2291-2305

[19] Christie FJ, Cassis G, Hochuli DF. Urbanisation affects the trophic structure of arboreal arthropod communities. Urban Ecosyst, 2010, 13(2): 169-180

[20] Clarke KR, Gorley RN, Somerfield PJ, Warwick RM (2014) Change in marine communities: an approach to statistical analysis and interpretation, 3nd edn. PRIMER-E, Plymouth

[21] Clarke KR, Gorley RN (2015) Getting started with PRIMER v7. PRIMER-E, Plymouth, Plymouth Marine Laboratory, 20

[22] Clarke KR. Non-parametric multivariate analyses of changes in community structure. Aust J Ecol, 1993, 18(1): 117-143

[23] Coley PD, Barone JA. Herbivores and plant defenses in tropical forests. Annu Rev Ecol Syst, 1996, 27(1): 305-335

[24] Damptey FG, de la Riva EG, Birkhofer K. Trade-offs and synergies between food and fodder production and other ecosystem services in an actively restored forest, natural forest and an agroforestry system in Ghana. Front for Global Chang, 2021, 4: 47

[25] Daniels B, Jedamski J, Ottermanns R, Ross-Nickoll M. A "plan bee" for cities: pollinator diversity and plant-pollinator interactions in urban green spaces. PLoS ONE, 2020, 15(7): e0235492

[26] Davis KF, Dalin C, DeFries R, Galloway JN, Leach AM, Mueller ND (2019) Sustainable pathways for meeting future food demand. In: Ferranti P, Berry EM, Anderson JR (eds) Encyclopedia of food security and sustainability, vol 3

[27] Delgado de la Flor YA, Perry KI, Turo KJ, Parker DM, Thompson JL, Gardiner MM. Local and landscape-scale environmental filters drive the functional diversity and taxonomic composition of spiders across urban greenspaces. J Appl Ecol, 2020, 57(8): 1570-1580

[28] Diehl E, Sereda E, Wolters V, Birkhofer K. Effects of predator specialisation, host plant and climate on biological control of aphids by natural enemies: a meta-analysis. J Appl Ecol, 2013, 50(1): 262-270

[29] Drillet Z, Fung TK, Leong RAT, Sachidhanandam U, Edwards P, Richards D. Urban vegetation types are not perceived equally in providing ecosystem services and disservices. Sustainability, 2020, 12(5): 2076

[30] Dufour-Pelletier S, Tremblay AJ, Hébert C, Lachat T, Ibarzabal J. Testing the effect of snag and cavity supply on deadwood-associated species in a managed boreal forest. Forests, 2020, 11(4): 424

[31] Duthie T (2018) An assessment of ecosystem services and disservices in urban community gardens in Berlin (Germany) and Cape Town (South Africa). Doctoral dissertation, University of Leipzig, Leipzig, Germany. Retrieved from https://core.ac.uk/download/pdf/226136519.pdf

[32] Ebeling A, Hines J, Hertzog LR, Lange M, Meyer ST, Simons NK, Weisser WW. Plant diversity effects on arthropods and arthropod-dependent ecosystem functions in a biodiversity experiment. Basic Appl Ecol, 2018, 26: 50-63

[33] Entling W, Schmidt MH, Bacher S, Brandl R, Nentwig W. Niche properties of Central European spiders: shading, moisture and the evolution of the habitat niche. Glob Ecol Biogeogr, 2007, 16(4): 440-448

[34] Ekström AL, Bergmark P, Hekkala AM. Can multifunctional forest landscapes sustain a high diversity of saproxylic beetles?. For Ecol Manag, 2021, 490: 119107

[35] Elmhagen B, Destouni G, Angerbjörn A, Borgström S, Boyd E, Cousins SA et al (2015) Interacting effects of change in climate, human population, land use, and water use on biodiversity and ecosystem services. Ecol Soc 20(1)

[36] Everett RA, Ruiz GM. Coarse woody debris as a refuge from predation in aquatic communities. Oecologia, 1993, 93(4): 475-486

[37] Feltynowski M, Kronenberg J. Urban green spaces—an underestimated resource in third-tier towns in Poland. Land, 2020, 9(11): 453

[38] Fenoglio MS, Rossetti MR, Videla M. Negative effects of urbanisation on terrestrial arthropod communities: a meta-analysis. Glob Ecol Biogeogr, 2020, 29(8): 1412-1429

[39] Frimpong BF, Molkenthin F. Tracking urban expansion using random forests for the classification of landsat imagery (1986–2015) and predicting urban/built-up areas for 2025: A Study of the Kumasi Metropolis, Ghana. Land, 2021, 10(1): 44

[40] Gardner TA, Barlow J, Chazdon R, Ewers RM, Harvey CA, Peres CA, Sodhi NS. Prospects for tropical forest biodiversity in a human-modified world. Ecol Lett, 2009, 12(6): 561-582

[41] Gerlach J, Samways M, Pryke J. Terrestrial invertebrates as bioindicators: an overview of available taxonomic groups. J Insect Conserv, 2013, 17(4): 831-850

[42] Gómez-Cifuentes A, Munevar A, Gimenez VC, Gatti MG, Zurita GA. Influence of land use on the taxonomic and functional diversity of dung beetles (Coleoptera: Scarabaeinae) in the southern Atlantic forest of Argentina. J Insect Conserv, 2017, 21(1): 147-156

[43] Grodsky SM, Moorman CE, Fritts SR, Campbell JW, Sorenson CE, Bertone MA, Wigley TB. Invertebrate community response to coarse woody debris removal for bioenergy production from intensively managed forests. Ecol Appl, 2018, 28(1): 135-148

[44] Güneralp B, Seto KC (2013) Sub-regional assessment of China: urbanisation in biodiversity hotspots. In: Urbanization, biodiversity and ecosystem services: challenges and opportunities. Springer, Dordrecht, pp 57–63

[45] Haeler E, Bergamini A, Blaser S, Ginzler C, Hindenlang K, Keller C, Lachat T. Saproxylic species are linked to the amount and isolation of dead wood across spatial scales in a beech forest. Landsc Ecol, 2021, 36(1): 89-104

[46] Ho J, Tumkaya T, Aryal S, Choi H, Claridge-Chang A. Moving beyond P values: data analysis with estimation graphics. Nat Methods, 2019, 16(7): 565-566

[47] Hodkinson ID, Jackson JK. Terrestrial and aquatic invertebrates as bioindicators for environmental monitoring, with particular reference to mountain ecosystems. Environ Manag, 2005, 35(5): 649-666

[48] Husch B, Beers T, Kershaw J Jr Forest mensuration, 2003 Hoboken Willey

[49] Ives CD, Lentini PE, Threlfall CG, Ikin K, Shanahan DF, Garrard GE, Kendal D. Cities are hotspots for threatened species. Glob Ecol Biogeogr, 2016, 25(1): 117-126

[50] Jouveau S, Toïgo M, Giffard B, Castagneyrol B, Van Halder I, Vétillard F, Jactel H. Carabid activity-density increases with forest vegetation diversity at different spatial scales. Insect Conserv Divers, 2020, 13(1): 36-46

[51] Keroumi AE, Naamani K, Soummane H, Dahbi A. Seasonal dynamics of ant community structure in the Moroccan Argan Forest. J Insect Sci, 2012, 12(1): 94

[52] Khanaposhtani MG, Kaboli M, Karami M, Etemad V. Effect of habitat complexity on richness, abundance and distributional pattern of forest birds. Environ Manag, 2012, 50(2): 296-303

[53] Koivula MJ. Useful model organisms, indicators, or both? Ground beetles (Coleoptera, Carabidae) reflecting environmental conditions. ZooKeys, 2011, 100: 287

[54] Kowarik I, Fischer LK, Kendal D (2020) Biodiversity conservation and sustainable urban development. Sustainability 12(12):4964

[55] Latha T, Sabu TK. Effects of land use change on dung beetle (Scarabaeinae) community structure in South Western Ghats. Int J Environ Agric Biotechnol, 2019, 4: 198-208

[56] Lassau SA, Hochuli DF, Cassis G, Reid CA. Effects of habitat complexity on forest beetle diversity: do functional groups respond consistently?. Divers Distrib, 2005, 11(1): 73-82

[57] Le Provost G, Badenhausser I, Le Bagousse-Pinguet Y, Clough Y, Henckel L, Violle C, Gross N. Land-use history impacts functional diversity across multiple trophic groups. Proc Natl Acad Sci, 2020, 117(3): 1573-1579

[58] Lee CM, Kwon TS. Response of ground arthropods to effect of urbanisation in southern Osaka, Japan. J Asia-Pac Biodivers, 2015, 8(4): 343-348

[59] Leschen RA, Carlton CE. Debris cloaking in endomychidae: a new species from Peru (Coleoptera). Zool J Linn Soc, 1993, 109(1): 35-51

[60] Majka CG. The erotylidae and endomychidae (Coleoptera: Cucujoidea) of the maritime Provinces of Canada: new records, zoogeography, and observations on beetle-fungi relationships and forest health. Zootaxa, 2007, 1546(1): 39-50

[61] Mata L, Andersen AN, Morán-Ordóñez A, Hahs AK, Backstrom A, Ives CD, Lynch Y (2020) Indigenous plants promote insect biodiversity in urban greenspaces. bioRxiv

[62] Mata L, Threlfall CG, Williams NS, Hahs AK, Malipatil M, Stork NE, Livesley SJ. Conserving herbivorous and predatory insects in urban green spaces. Sci Rep, 2017, 7(1): 1-12

[63] McIntyre NE. Ecology of urban arthropods: a review and a call to action. Ann Entomol Soc Am, 2000, 93(4): 825-835

[64] McPhearson T, Karki M, Herzog C, Santiago Fink H, Abbadie L, Kremer P, Dubbeling M (2018) Urban ecosystems and biodiversity. Urban Climate Change Research Network second assessment report on climate change in cities (ARC3–2). Cambridge University Press, Cambridge

[65] Méndez-Rojas DM, Cultid-Medina C, Escobar F. Influence of land use change on rove beetle diversity: a systematic review and global meta-analysis of a mega-diverse insect group. Ecol Ind, 2021, 122: 107239

[66] Mensah CA, Andres L, Perera U, Roji A (2016) Enhancing quality of life through the lens of green spaces: a systematic review approach. Int J Wellbeing 6(1)

[67] Mestre L, Jansson N, Ranius T. Saproxylic biodiversity and decomposition rate decrease with small-scale isolation of tree hollows. Biol Cons, 2018, 227: 226-232

[68] Mollot G, Pantel JH, Romanuk TN. The effects of invasive species on the decline in species richness: a global meta-analysis. Adv Ecol Res, 2017, 56: 61-83

[69] Muller JN, Loh S, Braggion L, Cameron S, Firn JL. Diverse urban plantings managed with sufficient resource availability can increase plant productivity and arthropod diversity. Front Plant Sci, 2014, 5: 517

[70] Nichols E, Larsen T, Spector S, Davis AL, Escobar F, Favila M, Network TSR. Global dung beetle response to tropical forest modification and fragmentation: a quantitative literature review and meta-analysis. Biol Cons, 2007, 137(1): 1-19

[71] Norton BA, Evans KL, Warren PH. Urban biodiversity and landscape ecology: patterns, processes and planning. Curr Landsc Ecol Rep, 2016, 1: 178-192

[72] Nyffeler M, Birkhofer K. An estimated 400–800 million tons of prey are annually killed by the global spider community. Sci Nat, 2017, 104(3–4): 30

[73] O'Brien MJ, Brezzi M, Schuldt A, Zhang JY, Ma K, Schmid B, Niklaus PA. Tree diversity drives diversity of arthropod herbivores, but successional stage mediates detritivores. Ecol Evol, 2017, 7(21): 8753-8760

[74] Oksanen J. Multivariate analysis of ecological communities in R: vegan tutorial. R Package Ver, 2011, 1(7): 1-43

[75] Oliver TH, Isaac NJ, August TA, Woodcock BA, Roy DB, Bullock JM. Declining resilience of ecosystem functions under biodiversity loss. Nat Commun, 2015, 6(1): 1-8

[76] Owusu K, Obour PB, Asare-Baffour S (2015) Climate variability and climate change impacts on smallholder farmers in the Akuapem North District, Ghana. In: Handbook of climate change adaptation. Springer, Berlin, Heidelberg, pp 1791–1806

[77] Parisi F, Pioli S, Lombardi F, Fravolini G, Marchetti M, Tognetti R. Linking deadwood traits with saproxylic invertebrates and fungi in European forests-a review. iForest-Biogeosci for, 2018, 11(3): 423

[78] Pauchard A, Aguayo M, Peña E, Urrutia R. Multiple effects of urbanisation on the biodiversity of developing countries: the case of a fast-growing metropolitan area (Concepción, Chile). Biol Cons, 2006, 127(3): 272-281

[79] Pielou EC. Ecological diversity, 1975 New York Wiley viii+165

[80] Planchuelo G, von Der Lippe M, Kowarik I. Untangling the role of urban ecosystems as habitats for endangered plant species. Landsc Urban Plan, 2019, 189: 320-334

[81] Potapov AM, Dupérré N, Jochum M, Dreczko K, Klarner B, Barnes AD, Scheu S. Functional losses in ground spider communities due to habitat structure degradation under tropical land-use change. Ecology, 2020, 101(3): e02957

[82] Prieto-Benítez S, Méndez M. Effects of land management on the abundance and richness of spiders (Araneae): a meta-analysis. Biol Cons, 2011, 144(2): 683-691

[83] R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing. ISBN 3–900051–07–0.

[84] Ramos DL, Cunha WL, Evangelista J, Lira LA, Rocha MVC, Gomes PA, Togni PHB. Ecosystem services provided by insects in Brazil: what do we really know?. Neotrop Entomol, 2020, 49: 783-794

[85] Sattler T, Duelli P, Obrist MK, Arlettaz R, Moretti M. Response of arthropod species richness and functional groups to urban habitat structure and management. Landsc Ecol, 2010, 25(6): 941-954

[86] Schiegg K. Effects of dead wood volume and connectivity on saproxylic insect species diversity. Ecoscience, 2000, 7(3): 290-298

[87] Schowalter T. Arthropod diversity and functional importance in old-growth forests of North America. Forests, 2017, 8(4): 97

[88] Schuldt A, Ebeling A, Kunz M, Staab M, Guimarães-Steinicke C, Bachmann D, Eisenhauer N. Multiple plant diversity components drive consumer communities across ecosystems. Nat Commun, 2019, 10(1): 1-11

[89] Sebek P, Vodka S, Bogusch P, Pech P, Tropek R, Weiss M, Cizek L. Open-grown trees as key habitats for arthropods in temperate woodlands: the diversity, composition, and conservation value of associated communities. For Ecol Manag, 2016, 380: 172-181

[90] Seibold SK (2015) Biodiversity of deadwood dependent insects–effects of forest management and prospects of conservation (Doctoral dissertation, Technische Universität München)

[91] Seibold S, Thorn S (2018) The importance of deadwood amount for saproxylic insects and how it interacts with deadwood diversity and other habitat factors. In: Saproxylic insects. Springer, Cham, pp 607–637

[92] Seto KC, Güneralp B, Hutyra LR. Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. Proc Natl Acad Sci, 2012, 109(40): 16083-16088

[93] Shannon CE. A mathematical theory of communication. Bell Syst Tech J, 1948, 27(3): 379-423

[94] Shochat E, Stefanov WL, Whitehouse MEA, Faeth SH. Spider diversity in the greater Phoenix area: the influence of human modificationof habitat structure and productivity. Ecol Appl, 2004, 14: 268-280

[95] Simpson EH. Measurement of diversity. Nature, 1949, 163(4148): 688-688

[96] Sokal RR, Rohlf FJ. Introduction to biostatistics, 1987 2 New York Freeman

[97] Staab M, Schuldt A (2020) The influence of tree diversity on natural enemies—a review of the “enemies” hypothesis in forests. Curr For Rep 1–17

[98] Štokmane M, Spungis V. The influence of vegetation structure on spider species richness, diversity and community organisation in the Apšuciems calcareous fen, Latvia. Anim Biodivers Conserv, 2016, 39(2): 221-236

[99] Susilo FX, Indriyati I, Hardiwinoto S (2009) Diversity and abundance of beetle (Coleoptera) functional groups in a range of land use system in Jambi, Sumatra. Biodivers J Biol Divers 10(4)

[100] Ulyshen MD, Hanula JL. Habitat associations of saproxylic beetles in the southeastern United States: a comparison of forest types, tree species and wood postures. For Ecol Manag, 2009, 257(2): 653-664

[101] Underwood EC, Quinn JF. Response of ants and spiders to prescribed fire in oak woodlands of California. J Insect Conserv, 2010, 14(4): 359-366

[102] Vargas-Hernández JG, Zdunek-Wielgołaska J. Urban green infrastructure as a tool for controlling the resilience of urban sprawl. Environ Dev Sustain, 2021, 23(2): 1335-1354

[103] Wang X, Hua F, Wang L, Wilcove DS, Yu DW. The biodiversity benefit of native forests and mixed-species plantations over monoculture plantations. Divers Distrib, 2019, 25(11): 1721-1735

[104] Wende B, Gossner MM, Grass I, Arnstadt T, Hofrichter M, Floren A, Steffan-Dewenter I. Trophic level, successional age and trait matching determine specialisation of deadwood-based interaction networks of saproxylic beetles. Proc R Soc B Biol Sci, 2017, 284(1854): 20170198

[105] Wenninger EJ, Inouye RS. Insect community response to plant diversity and productivity in a sagebrush–steppe ecosystem. J Arid Environ, 2008, 72(1): 24-33

[106] Wiafe E. Patterns of tropical tree species richness along elevational gradients of Mountain Afadjato, Ghana. Eur J for Sci, 2014, 2(2): 18-23

[107] Zanetti NI. Records of epigeal spiders in Bahia Blanca in the temperate region of Argentina. Acta Zool Mex, 2016, 32(1): 32-44

Funding

Brandenburgische TU Cottbus-Senftenberg (5408)