Advertisement

Journal of Insect Conservation

, Volume 18, Issue 5, pp 885–894 | Cite as

Conserving insect assemblages in urban landscapes: accounting for species-specific responses and imperfect detection

  • Luis Mata
  • Marta Goula
  • Amy K. Hahs
ORIGINAL PAPER

Abstract

Understanding how global environmental change impacts insect biodiversity is central to the core principals of conservation biology. To preserve the ecosystem services provided by insects in cities, it is crucial to understand how insect species are influenced by the degree of urbanization of the surrounding landscape. Using a hierarchical occupancy–detection model, we estimated the effect of urbanization on heteropteran bug species richness and occupancy, an approach that concurrently accounts for species-specific responses and imperfect detection. We found that species richness decreased along a gradient of increasing urbanization. This trend corresponded well with species-specific trends, as approximately two-thirds of all herbivores and predatory species experienced a strong mean negative response to urbanization. These results indicate that many species are potentially at risk of local extinction as cities grow and expand in the future. A second group of species, however, showed a weak mean negative response, indicating that they are ubiquitous urban species that thrive regardless of the surrounding degree of urban disturbance. Our research suggests that as cities develop, many of the species that are currently present will become less likely to occur, and therefore assemblages in the future are likely to become more simplified. In order to preserve or increase insect biological diversity in cities, it is critical to understand how individual species are influenced by urbanization. Our finding that insects display species-specific responses to urbanization has important repercussions for decision makers charged with preserving and improving urban biodiversity and the deliverance of ecosystem services in cities.

Keywords

Bayesian inference Heteropteran bugs Hierarchical models Imperfect detection Species-specific responses Urban ecology 

Notes

Acknowledgments

The authors wish to thank Helena Casellas, Josep Solà and Araceli Torró for their assistance during field work, landscape characterization, insect sorting and heteropteran bug identification. We also thank Gurutzeta Guillera-Arroita and Jose Lahoz-Monfort for their help with the statistical model. Field work was partially supported by the ‘Emerging Research Groups Funding Program’ (Faculty of Biology, University of Barcelona). LM wishes to acknowledge the support of funding from the Agència de Gestió d’Ajuts Universitaris i de Recerca (AGAUR), the Australian Government’s national Environmental Research Program (NERP) and the Australian Research Council Centre of Excellence for Environmental Decisions (CEED). AKH would like to acknowledge financial support from the Baker Foundation. The manuscript greatly benefited from the comments from three anonymous reviewers.

Supplementary material

10841_2014_9696_MOESM1_ESM.zip (192 kb)
Supplementary material 1 (ZIP 192 kb)
10841_2014_9696_MOESM2_ESM.zip (18 kb)
Supplementary material 2 (ZIP 19 kb)

References

  1. Adler PH, Foottit RG (2009) Introduction. In: Foottit R, Adler P (eds) Insect biodiversity: science and society. Wiley, Chichester, pp 1–6CrossRefGoogle Scholar
  2. Alomar O, Widenmann R (eds) (1999) Zoophytophagous Heteroptera: implications for life history and integrated pest management. Entomological Society of America, MarylandGoogle Scholar
  3. Ambrose DP (2000) Assassin bugs (Reduviidae excluding Triatominae). In: Schaefer CW, Panizzi AR (eds) Heteroptera of economic importance. CRC Press, Boca Raton, pp 695–712CrossRefGoogle Scholar
  4. Berenbaum M (1996) Bugs in the system: insects and their impact on human affairs. Helix Books, CambridgeGoogle Scholar
  5. Braman SK (2000) Damsel bugs (Nabidae). In: Schaefer CW, Panizzi AR (eds) Heteroptera of economic importance. CRC Press, Boca Raton, pp 639–656CrossRefGoogle Scholar
  6. Cardinale B, Duffy J, Gonzalez A, Hooper D, Perrings C, Venail P, Narwani A, Mace G, Tilman D, Wardle D, Kinzig A, Daily G, Loreau M, Grace J, Larigauderie A, Srivastava D, Naem S (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67PubMedCrossRefGoogle Scholar
  7. Catterall CP (2009) Responses of faunal assemblages to urbanization: global research paradigms and an avian case study. In: McDonnell M, Hahs AK, Breuste J (eds) Ecology of cities and towns: a comparative approach. Cambridge University Press, Cambridge, pp 129–155CrossRefGoogle Scholar
  8. Coll M, Guershon M (2002) Omnivory in terrestrial arthropods: mixing plant and prey diets. Annu Rev Entomol 47:267–297PubMedCrossRefGoogle Scholar
  9. Dorazio R, Royle J (2005) Estimating size and composition of biological communities by modeling the occurrence of species. J Am Statist Assoc 100:389–398CrossRefGoogle Scholar
  10. Dorazio R, Royle J, Söderström B, Glimskär A (2006) Estimating species richness and accumulation by modeling species occurrence and detectability. Ecology 87:842–854PubMedCrossRefGoogle Scholar
  11. Duffy J (2009) Why biodiversity is important to the functioning of real-world ecosystems. Front Ecol Environ 7:437–444CrossRefGoogle Scholar
  12. Dunn RR (2005) Modern insect extinctions, the neglected majority. Conserv Biol 19:1030–1036CrossRefGoogle Scholar
  13. Elmqvist T, Fragkias M, Goodness J, Güneralp B, Marcotullio PJ, McDonald RI, Parnell S, Schewenius M, Sendstad M, Seto KC, Wilkinson C, Alberti M, Folke C, Frantzeskaki N, Haase D, Katti M, Nagendra H, Niemelä J, Pickett STA, Redman CL, Tidball K (2013) Stewardship of the biosphere in the urban era. In: Elmqvist T, Fragkias M, Goodness J, Güneralp B, Marcotullio PJ, McDonald RI, Parnell S, Schewenius M, Sendstad M, Seto KC, Wilkinson C (eds) Urbanization, biodiversity and ecosystem services: challenges and opportunities. Springer, Dordrecht, pp 719–746Google Scholar
  14. Estes J, Terborgh J, Brashares J, Power M, Berger J, Bond W, Carpenter S, Essington T, Holt R, Jackson J, Marquis R, Oksanen L, Oksanen T, Paine R, Pikitch E, Ripple W, Sandin S, Scheffer M, Schoener T, Shurin J, Sinclair A, Soulé M, Virtanen R, Wardle D (2011) Trophic downgrading of planet earth. Science 333:301–306PubMedCrossRefGoogle Scholar
  15. Eubanks M, Styrsky J, Denno R (2003) The evolution of omnivory in heteropteran insects. Ecology 84:2549–2556CrossRefGoogle Scholar
  16. Faeth SH, Bang C, Saari S (2011) Urban biodiversity: patterns and mechanisms. Ann NY Acad Sci 1223:69–81PubMedCrossRefGoogle Scholar
  17. Fischer J, Lindenmayer DB, Cowling A (2004) The challenge of managing multiple species at multiple scales: reptiles in an Australian grazing landscape. J Appl Ecol 41:32–44CrossRefGoogle Scholar
  18. Fischer J, Cleeton S, Lyons T, Miller J (2012) Urbanization and the predation paradox: the role of trophic dynamics in structuring vertebrate communities. Bioscience 69:809–818Google Scholar
  19. Gaston K (2010) Urbanization. In: Gaston K (ed) Urban ecology. Cambridge University Press, Cambridge, pp 10–34CrossRefGoogle Scholar
  20. Gelman A, Hill J (2007) Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, CambridgeGoogle Scholar
  21. Hahs AK, McDonnell M (2006) Selecting independent measures to quantify Melbourne’s urban-rural gradient. Landsc Urban Plan 78:435–448CrossRefGoogle Scholar
  22. Hahs AK, McDonnell M, Breuste J (2009) A comparative ecology of cities and towns: synthesis of opportunities and limitations. In: McDonnell M, Hahs AK, Breuste J (eds) Ecology of cities and towns: a comparative approach. Cambridge University Press, Cambridge, pp 574–596CrossRefGoogle Scholar
  23. Henry T (2009) Biodiversity of Heteroptera. In: Foottit R, Adler P (eds) Insect biodiversity—science and society. Wiley, Chichester, pp 223–263CrossRefGoogle Scholar
  24. Hornung E, Tóthmérész B, Magura T, Vilisics F (2007) Changes of isopod assemblages along an urban-suburban-rural gradient in Hungary. Eur J Soil Bio 43:158–165CrossRefGoogle Scholar
  25. Horváth R, Magura T, Tóthmérész B (2012) Ignoring ecological demands masks the real effect of urbanization: a case study of ground-dwelling spiders along a rural–urban gradient in a lowland forest in Hungary. Ecol Res 27:1069–1077CrossRefGoogle Scholar
  26. Iknayan KJ, Tingley MW, Furnas BJ, Beissinger SR (2014) Detecting diversity: emerging methods to estimate species diversity. Trends Ecol Evol 29:97–106PubMedCrossRefGoogle Scholar
  27. Institut Cartogràfic de Catalunya (2011) http://www.icc.es. Accessed 25 Feb 2014
  28. Institut d’Estadística de Catalunya (2010) http://idescat.cat. Accessed 25 Feb 2014
  29. Kéry M (2010) Introduction to WinBUGS for ecologists. A Bayesian approach to regression, ANOVA, mixed models and related analyses. Academic Press, BurlingtonGoogle Scholar
  30. Kéry M (2011) Towards the modelling of true species distributions. J Biogeogr 38:617–618CrossRefGoogle Scholar
  31. Kéry M, Royle J (2008) Hierarchical Bayes estimation of species richness and occupancy in spatially replicated surveys. J Appl Ecol 45:589–598CrossRefGoogle Scholar
  32. Kotze J, Venn S, Niemelä J, Spence J (2011) Effects of urbanization on the ecology and evolution of arthropods. In: Niemelä J (ed) Urban ecology, patterns processes and applications. Oxford University Press, New York, pp 159–166CrossRefGoogle Scholar
  33. Kremen C, Chaplin-Kremer R (2007) Insects as providers of ecosystem services: crop pollination and pest control. In: Stewart A, New T, Lewis O (eds) Insect conservation biology: proceedings of the royal entomological society’s 23rd symposium. CABI Publishing, Wallingford, pp 349–382CrossRefGoogle Scholar
  34. Lahoz-Monfort JJ, Guillera-Arroita G, Wintle BA (2013) Imperfect detection impacts the performance of species distribution models. Global Ecol Biogeogr. doi: 10.1111/geb.12138 Google Scholar
  35. Lattin JD (1999) Bionomics of the anthocoridae. Annu Rev Entomol 44:207–231PubMedCrossRefGoogle Scholar
  36. Lattin JD (2000) Minute pirate bugs (Anthocoridae). In: Schaefer CW, Panizzi AR (eds) Heteroptera of economic importance. CRC Press, Boca Raton, pp 607–637CrossRefGoogle Scholar
  37. Levin S (1999) Fragile dominion. Perseus Books, ReadingGoogle Scholar
  38. Losey J, Vaughan M (2006) The economic value of ecological services provided by insects. Bioscience 56:311–323CrossRefGoogle Scholar
  39. Luck G, Smallbone L (2010) Species diversity and urbanization: patterns, drivers and implications. In: Gaston K (ed) Urban ecology. Cambridge University Press, Cambridge, pp 88–119CrossRefGoogle Scholar
  40. Lunn D, Spiegelhalter D, Thomas A, Best N (2009) The BUGS project: evolution, critique and future directions. Stat Med 28:3049–3067PubMedCrossRefGoogle Scholar
  41. MacKenzie D, Nichols J, Royle A, Pollock K, Hines J, Bailey L (2006) Occupancy estimation and modeling: inferring patterns and dynamics of species occurrence. Elsevier, San DiegoGoogle Scholar
  42. Magura T, Lövei GL, Tóthmérész B (2010) Does urbanization decrease diversity in ground beetle (Carabidae) assemblages? Global Ecol Biogeogr 19:16–26CrossRefGoogle Scholar
  43. Magura T, Nagy D, Tóthmérész B (2013) Rove beetles respond heterogeneously to urbanization. J Insect Conserv 17:715–724CrossRefGoogle Scholar
  44. McCarthy M (2007) Bayesian methods for ecology. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  45. McDonnell M, Pickett S (1990) Ecosystem structure and function along urban–rural gradients: an unexploited opportunity for ecology. Ecology 71:1232–1237CrossRefGoogle Scholar
  46. McDonnell M, Hahs AK (2008) The use of gradient analysis studies in advancing our understanding of the ecology of urbanizing landscapes: current status and future directions. Landsc Ecol 23:1143–1155CrossRefGoogle Scholar
  47. McDonnell M, Hahs AK (2013) The future of urban biodiversity research: moving beyond the ‘low-hanging fruit’. Urban Ecosyst 16:397–409CrossRefGoogle Scholar
  48. McIntyre N (2000) Ecology of urban arthropods: a review and a call to action. Ann Entomol Soc Am 98:825–835CrossRefGoogle Scholar
  49. McIntyre N, Rango J (2009) Arthropods in urban ecosystems: community patterns as functions of anthropogenic land use. In: McDonnell M, Hahs AK, Breuste J (eds) Ecology of cities and towns: a comparative approach. Cambridge University Press, Cambridge, pp 233–242CrossRefGoogle Scholar
  50. McKinney M (2002) Urbanization, biodiversity, and conservation. Bioscience 52:883–889CrossRefGoogle Scholar
  51. McKinney M (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127:247–260CrossRefGoogle Scholar
  52. McKinney M (2008) Effects of urbanization on species richness: a review of plants and animals. Urban Ecol 11:161–176CrossRefGoogle Scholar
  53. McKinney M (2010) Urban futures. In: Gaston K (ed) Urban ecology. Cambridge University Press, Cambridge, pp 287–308CrossRefGoogle Scholar
  54. Moir ML, Vesk PA, Brennan KE, Keith DA, McCarthy MA, Hughes L (2011) Identifying and managing threatened invertebrates through assessments of coextinction risk. Conserv Biol 25:787–796PubMedCrossRefGoogle Scholar
  55. New TR (2009) Insect species conservation. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  56. Niemelä J, Kotze J (2009) Carabid beetle assemblages along urban to rural gradients: a review. Landsc Urban Plan 92:65–71CrossRefGoogle Scholar
  57. Perdikis D, Fantinou A, Lykouressis D (2011) Enhancing pest control in annual crops by conservation of predatory Heteroptera. Biol Control 59:13–21CrossRefGoogle Scholar
  58. Pickett S, Cadenasso M, Grove J, Boone C, Groffman P, Irwin E, Kaushal S, Marshall V, McGrath B, Nilon C, Pouyat R, Szlavecz K, Troy A, Warren P (2011) Urban ecological systems: scientific foundations and a decade of progress. J Environ Manage 92:331–362PubMedCrossRefGoogle Scholar
  59. Pimm SL, Raven P (2000) Biodiversity—extinction by numbers. Nature 403:843–845PubMedCrossRefGoogle Scholar
  60. Pimm SL, Russell G, Gittleman J, Brooks T (1995) The future of biodiversity. Nature 269:347–350Google Scholar
  61. Royle J, Dorazio R (2008) Hierarchical modeling and inference in ecology. The analysis of data from populations, metapopulations and communities. Academic Press, LondonGoogle Scholar
  62. Sala OE, Chapin FS, 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 287:1770–1774PubMedCrossRefGoogle Scholar
  63. Samways MJ (2007) Insect conservation: a synthetic management approach. Annu Rev Entomol 52:465–487PubMedCrossRefGoogle Scholar
  64. Sattler T, Duelli P, Obrist M, Arlettaz R, Moretti M (2010) Response of arthropod species richness and functional groups to urban habitat structure and management. Landsc Ecol 25:941–954CrossRefGoogle Scholar
  65. Schaefer CW, Kotulski J (2000) Scentless plant bugs (Rhopalidae). In: Schaefer CW, Panizzi AR (eds) Heteroptera of economic importance. CRC Press, Boca Raton, pp 309–319CrossRefGoogle Scholar
  66. Schaefer CW, Panizzi AR (2000) Economic importance of Heteroptera: a general view. In: Schaefer CW, Panizzi AR (eds) Heteroptera of economic importance. CRC Press, Boca Raton, pp 3–8CrossRefGoogle Scholar
  67. Schuh R, Slater J (1995) True bugs of the world (Hemiptera: Heteroptera). Classification and natural history. Cornell University Press, IthacaGoogle Scholar
  68. Scudder G (2009) The importance of insects. In: Foottit R, Adler P (eds) Insect biodiversity—science and society. Wiley, Chichester, pp 7–32CrossRefGoogle Scholar
  69. Servei Meteorològic de Catalunya (2010) http://www.meteo.cat. Accessed 25 Feb 2014
  70. Seto KC, Parnell S, Elmqvist T (2013) A global outlook on urbanization. In: Elmqvist T, Fragkias M, Goodness J, Güneralp B, Marcotullio PJ, McDonald RI, Parnell S, Schewenius M, Sendstad M, Seto KC, Wilkinson C (eds) Urbanization, biodiversity and ecosystem services: challenges and opportunities. Springer, Dordrecht, pp 1–12Google Scholar
  71. Shreeve TG, Dennis RLH (2011) Landscape scale conservation: resources, behavior, the matrix and opportunities. J Insect Conserv 15:179–188CrossRefGoogle Scholar
  72. Stork N (2010) Re-assessing current extinction rates. Biodivers Conserv 19:357–371CrossRefGoogle Scholar
  73. Straub C, Finke D, Snyder W (2008) Are the conservation of natural enemy biodiversity and biological control compatible goals? Biol Control 45:225–237CrossRefGoogle Scholar
  74. Sturtz S, Ligges U, Gelman A (2005) R2WinBUGS: a package for running WinBUGS from R. J Stat Softw 12:1–16Google Scholar
  75. Sweet MH (2000) Seed and chinch bugs (Lygaeoidea). In: Schaefer CW, Panizzi AR (eds) Heteroptera of economic importance. CRC Press, Boca Raton, pp 143–264CrossRefGoogle Scholar
  76. Tóthmérész B, Máthé I, Balázs E, Magura T (2011) Responses of carabid beetles to urbanization in Transylvania (Romania). Landsc Urban Plan 101:330–337CrossRefGoogle Scholar
  77. Waldbauer G (2003) What good are bugs?. Harvard University Press, CambridgeGoogle Scholar
  78. Weeks J, Larson D, Fugate D (2005) Patterns of urban land use as assessed by satellite imagery: an application to Cairo, Egypt. In: Entwisle B, Rindfuss Stern P (eds) Population, land use, and environment: research directions. The National Academies Press, San Diego, pp 265–286Google Scholar
  79. Weirauch C, Schuh R (2011) Systematics and evolution of Heteroptera: 25 years of progress. Annu Rev Entomol 56:487–510PubMedCrossRefGoogle Scholar
  80. Wheeler AG (2000a) Plant bugs (Miridae) as plant pest. In: Schaefer CW, Panizzi AR (eds) Heteroptera of economic importance. CRC Press, Boca Raton, pp 37–83Google Scholar
  81. Wheeler AG (2000b) Predacious plant bugs (Miridae). In: Schaefer CW, Panizzi AR (eds) Heteroptera of economic importance. CRC Press, Boca Raton, pp 657–693CrossRefGoogle Scholar
  82. Wheeler AG, Hoebeke ER (2009) Adventive (non-native) insects: importance to science and society. In: Foottit R, Adler P (eds) Insect biodiversity—science and society. Wiley, Chichester, pp 475–521CrossRefGoogle Scholar
  83. Wilson E (1992) The diversity of life. Norton and Company, New YorkGoogle Scholar
  84. Wintle BA, Walshe T, Parris K, McCarthy MA (2012) Designing occupancy surveys and interpreting non-detection when observations are imperfect. Divers Distrib 18:417–424CrossRefGoogle Scholar
  85. Zipkin E, DeWan A, Royle A (2009) Impacts of forest fragmentation on species richness: a hierarchical approach to community modelling. J Appl Ecol 46:815–822CrossRefGoogle Scholar
  86. Zipkin E, Royle A, Dawson D, Bates S (2010) Multi-species occurrence models to evaluate the effects of conservation and management actions. Biol Conserv 143:479–484CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.Departament de Biologia AnimalUniversitat de BarcelonaBarcelonaSpain
  2. 2.Interdisciplinary Conservation Science Research Group, School of Global, Urban and Social StudiesRMIT UniversityMelbourneAustralia
  3. 3.Institut de Recerca de la BiodiversitatUniversitat of BarcelonaBarcelonaSpain
  4. 4.Australian Research Centre for Urban Ecology, Royal Botanic Gardens Melbourne c/o The School of BotanyThe University of MelbourneParkvilleAustralia

Personalised recommendations