Urbanization Affects Composition but Not Richness of Flower Visitors in the Yungas of Argentina


Urban areas represent a spatially small impact in relation to other land-uses such as livestock and agriculture, but they undergo rapid changes. Such changes involve their size, shape, interconnectivity, and composition of natural patches. Habitat loss generated by urbanization affects the diversity and abundance of bees and other flower visitors in many sites. In general, the presence of urban areas represents a strict boundary to flower visitors and restricts their movement between natural and suburban habitat patches. The aim of this work is to evaluate how the flower visitor assemblage change along an urban-natural gradient in northwest Argentina. We established five areas in the Yungas ecoregion and sampled three sites with different degrees of urbanization (urban, suburban, and natural), at each area, reaching 15 sites. At each site, we sampled flower visitors during 5-min observation periods done over flowering plants. We found 197 morphospecies of flower-visiting insects along the gradient and an invariant richness, abundance, and Shannon diversity. The assemblage presented the same taxonomic group distributions in the three categories established. However, in urban sites, solitary bees and bees with soil borrowing nesting type predominate, while eusocial and cavity nesting bees were the main flower visitors in suburban sites. Our results suggest that the cities of northwestern Argentina are not a strict boundary for flower visitors; however, urbanization seems to be selecting and favoring certain flower-visitor species traits.

This is a preview of subscription content, access via your institution.

Fig 1
Fig 2
Fig 3
Fig 4
Fig 5
Fig 6


  1. Ahrne K, Bengtsson J, Elmqvist T (2009) Bumble bees (Bombus spp) along a gradient of increasing urbanization. J Pak Med Assoc 67:1664–1669

    Google Scholar 

  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26(1):32–46

    Google Scholar 

  3. Anderson MJ, Walsh DC (2013) PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecol Monogr 83(4):557–574

    Article  Google Scholar 

  4. Añino Y, Parra-H A, Gálvez D (2019) Are orchid bees (Apidae: Euglossini) good indicators of the state of conservation of neotropical forests? Sociobiology 66(1):194–197

    Article  Google Scholar 

  5. Baldock KCR, Goddard MA, Hicks DM, Kunin WE, Mitschunas N, Osgathorpe LM, Potts S, Robertson KM, Scott AV, Stone GN, Vaughan IP and Memmott J (2015) Where is the UK’s pollinator biodiversity? The importance of urban areas for flower-visiting insects Proc R Soc B 282

  6. Banaszak-Cibicka W, Zmihorski M (2012) Wild bees along an urban gradient: winners and losers. J Insect Conserv 16:331–343

    Article  Google Scholar 

  7. Bates AJ, Sadler JP, Fairbrass AJ, Falk SJ, Hale JD, Matthews TJ (2011) Changing bee and hoverfly pollinator assemblages along an urban-rural gradient. PLoS One 6

  8. Biesmeijer JC, Roberts SPM, Reemer M, Ohlemüller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers R, Thomas CD, Settele J, Kunin WE (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science (New York, N.Y.) 313, 351–4

  9. Boldrini P, Malizia M (2017) Urbanizaciones informales en ciudades intermedias. Los casos del Gran San Salvador de Jujuy y Gran San Miguel de Tucumán (Noroeste argentino). CUADERNO URBANO. Espacio, cultura, sociedad 23(23):85–106

    Google Scholar 

  10. Brown A, Placci L, Grau N (1993) Ecología y diversidad de las selvas subtropicales de la Argentina. In Elementos de política ambiental (pp. 215-22)

  11. Brown A, Chalukian S, Malmierca L (1985) Estudio florístico-estructural de un sector de selva semidecidua del noroeste argentino. I: Composición florística, densidad y diversidad. Darwiniana 26:27–41

    Google Scholar 

  12. Brown AD, Ramadori E (1988) Patrón de distribución, diversidad y características ecológicas de las especies arbóreas de las selvas y bosques montanos del NO de la Argentina. In Actas VI Congreso Forestal Argentino Santiago del Estero pp 177–181

  13. Burdine JD, Mccluney KE (2019) Interactive effects of urbanization and local habitat characteristics influence bee communities and flower visitation rates. Oecologia 190(4):715–723

    Article  Google Scholar 

  14. Cabrera AL (1976) Regiones Fitogeográficas Argentinas, 2nd ed. Enciclopedia Argentina de Agricultura y Jardineria

  15. Cabrera AL, Willink A (1973) Biogeografía de América Latina. Organización de Estados Americanos, Washington, D.C.: Programa Regional de Desarrollo Científico y Tecnológico

  16. Chacoff NP, Vázquez DP, Lomáscolo SB, Stevani EL, Dorado J, Padrón B (2012) Evaluating sampling completeness in a desert plant–pollinator network. J Anim Ecol 81(1):190–200

    Article  Google Scholar 

  17. Chao A (1987) Estimating the population size for capture-recapture data with unequal catchability. Biometrics 783–791

  18. Chao A, Colwell RK, Lin CW, Gotelli NJ (2009) Sufficient sampling for asymptotic minimum species richness estimators. Ecology 90:1125–1133

    Article  Google Scholar 

  19. Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Philos Trans Royal Soc B 345:101–118

    CAS  Article  Google Scholar 

  20. Deguines N, Julliard R, de Flores M, Fontaine C (2012) The whereabouts of flower visitors: contrasting land-use preferences revealed by a country-wide survey based on citizen science. PLoS One 7(9)

  21. Dicks VL, Viana B, Bommarco R, Brosi B, Arizmendi M, Cunningham SA, Galetto L, Hill R, Lopes AV, Pires C, Taki H, Potts SG (2016) Ten policies for pollinators_ what governments can do to safeguard pollination services. Embrapa Recursos Genéticos e Biotecnologia-Artigo em periódico indexado (ALICE)

  22. Dressler RL (1968) Pollination by euglossine bees. Evolution, 202–210.

  23. Ellis EC, Goldewijk KK, Siebert S, Lightman D, Ramankutty N (2010) Anthropogenic transformation of the biomes, 1700 to 2000. Glob Ecol Biogeogr 19:589–606

  24. Fortel L, Henry M, Guilbaud L, Guirao AL, Kuhlmann M, Mouret H, Rollin O, Vaissière BE (2014) Decreasing abundance, increasing diversity and changing structure of the wild bee community (hymenoptera: anthophila) along an urbanization gradient. PLoS One 9(8)

  25. Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, Kremen C, Carvalheiro LG, Harder LD, Afik O, Bartomeus I, Benjamin F, Boreux V, Cariveau D, Chacoff NP, Dudenhöffer JH, Freitas BM, Ghazoul J, Greenleaf S, Hipólito J, Holzschuh A, Howlett B, Isaacs R, Javorek SK, Kennedy CM, Krewenka KM, Krishnan S, Mandelik Y, Mayfield MM, Motzke I, Munyuli T, Nault BA, Otieno M, Petersen J, Pisanty G, Potts SG, Rader R, Ricketts TH, Rundlöf M, Seymour CL, Schüepp C, Szentgyörgyi H, Taki H, Tscharntke T, Vergara CH, Viana BF, Wanger TC, Westphal C, Williams N, Klein AM (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339:1608–1611 http://science.sciencemag.org/content/sci/339/6127/1608.full.pdf

    CAS  Article  Google Scholar 

  26. Gathmann A, Tscharntke T (2002) Foraging ranges of solitary bees. J Anim Ecol 71:757–764

    Article  Google Scholar 

  27. Glaum P, Simao MC, Vaidya C, Fitch G, Iulinao B (2017) Big city Bombus: using natural history and land-use history to find significant environmental drivers in bumble-bee declines in urban development. R. Soc. Open Sci 4(5):170156

    Article  Google Scholar 

  28. Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391

    Article  Google Scholar 

  29. Goulson D, Lye GC, Darvill B (2008) Decline and conservation of bumble bees. Annu Rev Entomol 53:191–208

    CAS  Article  Google Scholar 

  30. Guenat S, Kunin WE, Dougill AJ, Dallimer M (2019) Effects of urbanisation and management practices on pollinators in tropical Africa. J Appl Ecol 56(1):214–224

    Article  Google Scholar 

  31. Hall DM, Camilo GR, Tonietto RK, Ollerton J, Ahrné K, Arduser M, Ascher JS, Baldock KCR, Fowler R, Frankie G, Goulson D, Gunnarsson B, Hanley ME, Jackson JI, Langellotto G, Lowenstein D, Minor ES, Philpott SM, Potts SG, Sirohi MH, Spevak EM, Stone GN, Threlfall CG (2017) The city as a refuge for insect pollinators. Conserv Biol 31:24–29

    Article  Google Scholar 

  32. Hernandez JL, Frankie GW, Thorp RW (2009) Ecology of urban bees: a review of current knowledge and directions for future study. Cities and the Environment 2:1–15

    Article  Google Scholar 

  33. The National Institute of Statistics and Censuses (INDEC 2010) Available from: https://www.indec.gob.ar/indec/web/Nivel3-Tema-2-41

  34. Jones EL, Leather SR (2013) Invertebrates in urban areas: a review. EJE 109(4):463–478

    Google Scholar 

  35. Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Evol Syst 29(1):83–112

    Article  Google Scholar 

  36. Kennedy CM, Lonsdorf E, Neel MC, Williams NM, Ricketts TH, Winfree R, Bommarco R, Brittain C, Burley AL, Cariveau D, Carvalheiro LG, Chacoff NP, Cunningham SA, Danforth BN, Dudenhöffer JH, Elle E, Gaines HR, Garibaldi LA, Gratton C, Holzschuh A, Isaacs R, Javorek SK, Jha S, Klein AM, Krewenka K, Mandelik Y, Mayfield MM, Morandin L, Neame LA, Otieno M, Park M, Potts SG, Rundlöf M, Saez A, Steffan-Dewenter I, Taki H, Viana BF, Westphal C, Wilson JK, Greenleaf SS, Kremen C (2013) A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol Lett 16:584–599

    Article  Google Scholar 

  37. Klein A-M, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007, 1608) Importance of pollinators in changing landscapes for world crops. Proc R Soc B 274:303–313

  38. Klemm, M. (1996) Man-made bee habitats in the anthropogenous landscape of central Europe-substitutes for threatened or destroyed riverine habitats?. In Linnean society symposium series (Vol. 18, pp. 17-34). Academic press limited

  39. Legendre P, Legendre L (1998) Numerical Ecology, 2nd ed. Elsevier Science, BV. Amsterdam. 852p

  40. Mantel N, Valand RS (1970) A technique of nonparametric multivariate analysis. Biometrics 547–558

  41. Mantel N (1967) Ranking procedures for arbitrarily restricted observation. Biometrics 65-78

  42. Mc Cune B, Mefford MJ (1999) Pc-Ord. Multivariate analysis of ecological data, version 4. MjM software design

  43. McIntyre NE (2000) Ecology of urban arthropods: a review and a call to action. Ann Entomol Soc Am 93:825–835

    Article  Google Scholar 

  44. McKinney ML (2006) Urbanization as a major cause of biotic homogenization. Biol Conserv 127:247–260

    Article  Google Scholar 

  45. Michener CD (2000) The bees of the world. Johns Hopkins University Press, Baltimore

    Google Scholar 

  46. Nates Parra G (2016) Iniciativa Colombiana de Polinizadores Capítulo Abejas

  47. Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326

    Article  Google Scholar 

  48. Owen SM, MacKenzie AR, Bunce RGH, Stewart HE, Donovan RG, Stark G, Hewitt CN (2006) Urban land classification and its uncertainties using principal component and cluster analyses: a case study for the UK west midlands. Landsc Urban Plan 78(4):311–321

    Article  Google Scholar 

  49. Oyarzabal M, Clavijo JR, Oakley LJ, Biganzoli F, Tognetti PM, Barberis IM, Maturo HM, Aragón MR, Campanello PI, Prado DE, Oesterheld M, Leon RJC (2018) Unidades de vegetación de la Argentina. Ecol Austral 28:040–063

    Article  Google Scholar 

  50. Perovic P, Trucco C, Tálamo A, Quiroga V, Ramallo D, Lacci A, Baungardner A, Mohr, F (2008) Guía técnica para el monitoreo de la biodiversidad. Programa de Monitoreo de Biodiversidad-Parque Nacional Copo, Parque y Reserva Provincial Copo, y Zona de Amortiguamiento. APN/GEF/BIRF. Salta, Argentina

  51. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353. https://doi.org/10.1016/j.tree.2010.01.007

    Article  Google Scholar 

  52. Potts SG, Imperatriz-Fonseca V, Ngo HT, Aizen MA, Biesmeijer JC, Breeze TD, Dicks LV, Garibaldi LA, Hill R, Settele J, Vanbergen AJ (2016) Safeguarding pollinators and their values to human well-being. Nature 540:220–229

    CAS  Article  Google Scholar 

  53. Quistberg RD, Bichier P, Philpott SM (2016) Landscape and local correlates of bee abundance and species richness in urban gardens. Environ Entomol 45:592–601

    Article  Google Scholar 

  54. R Core Team (2019) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.rproject.org/index.html

  55. Seto KC, Güneralp B, Hutyra LR (2012) Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. Proc Natl Acad Sci U S A 109:16083–16088

  56. Tscharntke T, Steffan-Dewenter I, Kruess A, Thies C (2002) Characteristics of insect populations on habitat fragments: a mini review. Ecol Res pp 229–239

  57. Vides-Almonacid R., Ayarde HR, Scrocchi GJ, Romero F, Boero C, Chani, JM (1998) Biodiversidad de Tucumán y el Noroeste argentino. Opera Lilloana, 43

  58. Williams NM, Crone EE, Roulston TH, Minckley RL, Packer L, Potts SG (2010) Ecological and life-history traits predict bee species responses to environmental disturbances. Biol Conserv 143:2280–2291

    Article  Google Scholar 

  59. Winfree R, Aguilar R, Vázquez DP, LeBuhn G, Aizen MA (2009) A meta-analysis of bees' responses to anthropogenic disturbance. Ecology 90(8):2068–2076

    Article  Google Scholar 

Download references


We would like to thank Dr. Mariano Lucia and Dr. Leopoldo Alvarez who helped with pollinator identification, Carlos Cabrera for the GIS analyses for providing the site classification and for the Yungas distribution map, two anonymous reviewer for their comment which helped to improve the manuscript, and Dra. Sofia Nanni who help with English language.


This manuscript was funded by a fellowship by CONICET and a grant from SIGMA Xi foundation. Alejandro A. Amado has a doctoral fellowship and Natacha P. Chacoff is a carrier researcher from CONICET.

Author information




All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by AADS and NPC. The first draft of the manuscript was written by AADS. NPC commented on previous versions of the manuscript and she read and approved the final manuscript.

Corresponding author

Correspondence to A. A. Amado De Santis.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Edited by Márcia M Maués – Embrapa

Electronic Supplementary Material


(DOCX 128 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Amado De Santis, A.A., Chacoff, N.P. Urbanization Affects Composition but Not Richness of Flower Visitors in the Yungas of Argentina. Neotrop Entomol 49, 568–577 (2020). https://doi.org/10.1007/s13744-020-00772-z

Download citation


  • Urban ecology
  • flower-visitor assembly
  • bee traits
  • Jujuy province