Multi-taxonomic diversity patterns in a neotropical green city: a rapid biological assessment

Abstract

The growing number of urban ecology studies has raised concern about the importance of comprehending the ecological patterns and processes of urban areas in order to manage and plan them properly. In this study, we performed a rapid descriptive ecological assessment of the biodiversity patterns in a neotropical mid-sized urban area from a multi-taxonomic approach, contrasting seven taxonomic groups (i.e., vascular plants, fungi, ants, butterflies, beetles, amphibians, birds) in areas with different degree of urbanization intensity. Results of this study show that diversity patterns differ depending on the taxonomic group; thus, it was not possible to generalize specific trends in species richness, abundance, and species composition because each taxon seems to respond differently to the process or level of urbanization. Our results also highlight the relevance of using multi-taxonomic approaches to understand the relationship between biodiversity and urban environments, and underline potential benefits and limitations of using each of the studied groups when considering rapid biodiversity assessments. Based on our results, we suggest the following recommendations when performing rapid biological assessments in urban areas: evaluate as many taxa as possible, choosing the set of taxonomic groups in relation to the objectives of the study, wide the temporal and spatial survey window as much as possible, focus on several biodiversity measures, and interpreting results cautiously, as rapid assessments do not necessarily reflect ecological patterns, but just part of the history.

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

Fig 1
Fig 2
Fig 3
Fig 4

References

  1. (CBD) Convention on Biological Diversity (2011) Aichi Biodiversity Targets. CBD, http://www.cbd.int/sp/targets/

  2. (INEGI) Instituto Nacional de Estadística, Geografía e Informática (2010) Censo Nacional de Población y Vivienda 2010. INEGI, Aguascalientes

  3. (PNUD) Programa de las Naciones Unidas para el Desarrollo (1996) Urban agriculture: Food, jobs and sustainable cities. PNUD, New York

  4. (UN) United Nations (2013) World urbanization prospects, the 2011 revision. http://esa.un.org/unup/

  5. (USAID) United States Agency for International Development (2010) Urbanization in Latin America and the Caribbean: Trends and challenges, Washington, D.C.

  6. Arenas-Cruz MA (2014) Diversidad de anfibios en áreas verdes urbanas de Xalapa. Veracruz, MSc Thesis, Instituto de Ecología, A.C., Xalapa

  7. Arnett RH, Thomas MC (2001) American beetles, volume I: Archostemata. Staphyliniformia. CRC Press, Boca Raton, Myxophaga, Adephaga, Polyphaga

    Google Scholar 

  8. Arnett RH, Thomas MC, Skelley PE, Frank JH (2002) American beetles, volume II: Polyphaga: Scarabaeoidea through Curculionoidea. CRC Press, Boca Raton

    Google Scholar 

  9. Benítez Badillo G (2011) Crecimiento de la población y expansión urbana de la ciudad de Xalapa, Veracruz y sus efectos sobre la vegetación y agroecosistemas. Ph D. Thesis, Colegio de Postgraduados - Instituto de Enseñanza e Investigación en Ciencias Agrícolas, Veracruz

  10. Berkowitz AR, Nilon CH, Hollweg KS (2003) The importance of understanding urban ecosystems: Themes. In: Berkowitz AR, Nilon CH, Hollweg KS (eds) Understanding urban ecosystems - A new frontier for science and education. Sringer-Verlag, New York, pp 15–17

    Google Scholar 

  11. Bessette AE, Bessette AR, Fischer SW (1997) Mushrooms of Northeastern North America. Syracuse University Press, Syracuse

    Google Scholar 

  12. Bestelmeyer BT, Agosti D, Alonso LE, Brandao CRF, Brown WL, Delabie JHC, Silvestre R (2000) Field techniques for the study of ground-dwelling ants: An overview, description, and evaluation. In: Agosti D, Majer JD, Alonso LE, Shultz TR (eds) Ants - Standard methods for measuring and monitoring biodiversity. Smithsonian Institution Press, Washington, pp 122–144

    Google Scholar 

  13. Blair RB (1999) Birds and butterflies along an urban gradient: Surrogate taxa for assessing biodiversity? Ecol Appl 9:164–170

    Article  Google Scholar 

  14. Bolton B (1994) Identification guide to the ant genera of the World. Harvard University Press, Cambridge

    Google Scholar 

  15. Borror DJ, Tripplehorn CA, Johnson NF (1989) An introduction to the study of insects. Saunders College Publishing, Philadelphia

    Google Scholar 

  16. Bräuniger C, Knapp S, Kühn I, Klotz S (2010) Testing taxonomic and landscape surrogates for biodiversity in an urban setting. Landsc Urban Plan 97:283–295

    Article  Google Scholar 

  17. Breitenbach J, Kränzlin F (1984) Fungi of Switzerland, volume 1. Ascomycetes. VerlagMykologia, Lucerne

    Google Scholar 

  18. Carbó-Ramírez P, Zuria I (2011) The value of small urban greenspaces for birds in a Mexican city. Landsc Urban Plan 100:213–222

    Article  Google Scholar 

  19. Carbó-Ramírez P, Romero-González e P, Zuria I (2011) Primer reporte para México de coloración aberrante (leucismo parcial) en cuitlacoche pico curvo (Toxostoma curvirostre). Huitzil 12:1–4

    Google Scholar 

  20. Castellanos-González A (2004) Distribución y abundancia de Polygonum capitatum BUCH-HAM. Ex D. Don en calles del centro histórico de Xalapa, Veracruz. BscThesis, Facultad de Biología, Universidad Veracruzana, Xalapa

  21. Castillo-Campos G (1991) Vegetación y flora del municipio de Xalapa. Veracruz. Instituto de Ecología A.C, Xalapa

    Google Scholar 

  22. Cervantes-Cornihs E, Zuria I, Castellanos I (2009) Depredación de nidos artificiales en cercas vivas de un sistema agro-urbano en Hidalgo, México. Interciencia 34:777–783

    Google Scholar 

  23. Chávez-Zichinelli CA, MacGregor-Fors I, Talamás-Rhoana P et al (2010) Stress responses of the house sparrow (Passer domesticus) to different urban land-uses. Landsc Urban Plan 98:183–189

  24. Clarke KR, Warwick RM (1999) The taxonomic distinctness measure of biodiversity: weighting of steplengths between hierarchical levels. Mar Ecol-ProgSer 184:21–29

    Article  Google Scholar 

  25. Clergeau P, Croci S, Jokimäki J et al (2006) Avifauna homogenisation by urbanisation: analysis at different European latitudes. Biol Conserv 127:336–344

    Article  Google Scholar 

  26. Colwell RK (2013) EstimateS: Statistical estimation of species richness and shared species from samples. Version 9. http://viceroy.eeb.uconn.edu/estimates. Accessed 4 Dec 2013

  27. Crawley MJ (2005) Statistics - An introduction using R. John Wiley, Hoboken

    Google Scholar 

  28. De’Ath G, Fabricius KE (2000) Classification and regression trees: a powerfull yet simple technique for ecological data analysis. Ecology 81:3178–3192

    Article  Google Scholar 

  29. Dennis RWG (1978) British ascomycetes. J. Cramer, Vaduz

    Google Scholar 

  30. Development Core Team R (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, Available at: http://www.r-project.org/

    Google Scholar 

  31. Gío-Argáez R, Hernández Ruiz I, Sáinz-Hernández E (1989) Ecología Urbana. CONACYT–SGDSDDF–SESIC-SEP–UNAM–Secretaría de Desarrollo Urbano y Ecología–UAM. México, D.F.

  32. Glassberg J (2007) A swift guide to the butterflies of Mexico and Central America. Sunstreak, Morristown

    Google Scholar 

  33. Gómez-Aíza L, Zuria I (2010) Aves visitantes a las flores de maguey (Agave salmiana) en una zona urbana del centro de México. Ornitol Neotrop 21:17–30

    Google Scholar 

  34. González-García FR, Straub JA, Lobato García A, MacGregor-Fors I (2014) Birds of a neotropical green city: an up-to-date review of the avifauna of the city of Xalapa with additional unpublished records. Urban Ecosystems. doi:10.1007/s11252-014-0370-3

  35. González-Oreja JA, Bonache-Regidor C, Buzo-Franco D, De la Fuente-Díaz Ordáz AA, Hernández-Santín L (2007) Caracterización ecológica de la avifauna de los parques urbanos de la Ciudad de Puebla (México). Ardeola 54:53–67

    Google Scholar 

  36. González-Oreja JA, Bonache-Regidor C, De La Fuente-Díaz-Ordaz AA (2010) Far from the noisy world? Modelling the relationships between park size, tree cover and noise levels in urban green spaces of the city of Puebla, Mexico. Interciencia 35:486–492

    Google Scholar 

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

    Google Scholar 

  38. Grimm NB, Faeth SH, Golubiewski NE, et al. (2008) Global change and the ecology of cities. Science (80) 319:756–760

  39. Hanssen J, Knudsen L (1982) Nordic Macromycetes 2. Nordsvanmp, Copenhague

    Google Scholar 

  40. Hernández Baz F, Llorente Bousquets JE, Luis Martínez A, Vargas Fernández I (2010) Las mariposas de Veracruz - Guía Ilustrada. Consejo Veracruzano de Investigación Ciencia y Desarrollo Tecnológico, Veracruz

  41. Heyer WR DMA, McDiarmid RW, Hayek LAC, Foster MS (1994) Measuring and monitoring biological diversity - Standard methods for amphibians. Smithsonian Institute Press, Washington, DC

    Google Scholar 

  42. Hogsden KL, Hutchinson TC (2004) Butterfly assemblages along a human disturbance gradient in Ontario, Canada. Can J Zool 82:739–748

    Article  Google Scholar 

  43. Hölldobler B, Wilson EO (1990) The Ants. Harvard University Press, Cambridge

    Google Scholar 

  44. Horak E (2005) Röhrlinge und Blätterpilze in Europa. Elsevier, Munich

    Google Scholar 

  45. Hough M (1998) Naturaleza y ciudad: Planificación urbana y procesos ecológicos. Editorial Gili, Barcelona

    Google Scholar 

  46. Jost L (2007) Partitioning diversity into independent alpha and beta components. Ecology 88:2427–2439

    Article  PubMed  Google Scholar 

  47. Jost L, Chao A, Chazdon RL (2011) Compositional similarity and β (beta) diversity. In: Gotelli NJ, Colwell RK (eds) In: Magurran AE, McGillBJ (eds) Frontiers in measuring biodiversity. Oxford University Press, New York, pp 66–87

    Google Scholar 

  48. Knight RL, Rust MK (1990) The urban ants of California with distribution note of imported species. Southwest Nat 15:167–178

    Google Scholar 

  49. Largent D (1973) How to identify mushrooms to genus I - Macroscopic features. Mad River Press, Eureka

    Google Scholar 

  50. Largent D, Johnson D, Watling R (1977) How to identify mushrooms to genus III - Microscopic features. Mad River Press, Eureka

  51. Lemoine R (2012) Cambios en la cobertura vegetal de la ciudad de Xalapa-Enríquez, Veracruz y zonas circundantes entre 1950 y 2010. Facultad de Biología, Universidad Veracruzana, Xalapa, Bsc Thesis

  52. Lodge JD, Ammirati JF, O’ Dell TE, Mueller GM (2004) Collecting and describing macrofungi. In: Mueller GM, Bills GF, Foster MS (eds) Biodiversity of fungi. Inventory and monitoring methods. Elsevier Academic Press, San Diego

    Google Scholar 

  53. López-Flores V, MacGregor-Fors I, Schondube JE (2009) Artificial nest predation along a neotropical urban gradient. Landsc Urban Plan 92:90–95

  54. Lot A, Chiang F (1986) Manual de herbario. Consejo Nacional de la Flora de México, México, D.F.

  55. Lyytimäki J, Petersen LK, Normander B, Bezák P (2008) Nature as a nuisance? Ecosystem services and disservices to urban lifestyle. Environ Sci 5:161–172

    Article  Google Scholar 

  56. MacGregor-Fors I (2008) Relation between habitat attributes and bird richness in a western Mexico suburb. Landsc Urban Plan 84:92–98

    Article  Google Scholar 

  57. MacGregor-Fors I (2010) How to measure the urban-wild land ecotone: Redefining ‘peri-urban’ areas. Ecol Res 25:883–887

    Article  Google Scholar 

  58. MacGregor-Fors I, Ortega-Álvarez R (2011) Fading from the forest: Bird community shifts related to urban park site-specific and landscape traits. Urb For Urban Gree 10:239–246

    Article  Google Scholar 

  59. MacGregor-Fors I, Ortega-Álvarez R (2013) Ecología urbana: Experiencias en América Latina. www1.inecol.edu.mx/libro_ecologia_urbana

  60. MacGregor-Fors I, Payton M (2013) Contrasting diversity values: statistical inferences based on overlapping confidence intervals. PLoS One 8:e56794

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  61. MacGregor-Fors I, Morales-Pérez L, Schondube JE (2010) Migrating to the city: Responses of neotropical migrant bird communities to urbanization. Condor 112:711–717

    Article  Google Scholar 

  62. MacGregor-Fors I, Hernández Ordoñez O, Ortega-Álvarez R (2013) Urban croaking: Diversity and distribution of anurans in a neotropical city. Urban Ecosyst 16:389–396

    Article  Google Scholar 

  63. MacKay WP, MacKay E (1989) A guide to the species identification of the New World ants. Sociobiology 16:3–47

    Google Scholar 

  64. Magurran AE, McGill (2011) Biological diversity: Frontiers in measurement and assessment. Oxford University Press, Oxford

    Google Scholar 

  65. Malagamba-Rubio A, MacGregor-Fors I, Pineda-López R (2013) Comunidades de aves en áreas verdes de la ciudad de Santiago de Querétaro, México. Ornitol Neotrop 24:371–386

  66. Maya-Elizarrarás E (2011) Aves explotadoras de áreas verdes urbanas: un ejemplo de la Zona Metropolitana de Guadalajara, Jalisco. Canto del Centzontle 2:104–109

    Google Scholar 

  67. McKinney ML (2002) Urbanization, biodiversity and conservation. Bioscience 52:883–890

    Article  Google Scholar 

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

    Article  Google Scholar 

  69. McKinney ML (2008) Do humans homogenize or differentiate biotas? It depends. J Biogeogr 35:1960–1961

    Article  Google Scholar 

  70. Moreno CE, Pineda E, Escobar F, Sánchez-Rojas G (2007) Shortcuts for biodiversity valuation: A review of terms and recommendations about the use of target groups, bioindicators and surrogates. Int J Environ Health 1:71–86

    Article  Google Scholar 

  71. Morón MA, Terrón RA (1988) Entomología Práctica. Instituto de Ecología A.C., México, D.F.

  72. Mueller GM, Bills GF, Foster SM (2004) Biodiversity of fungi: Inventory and monitoring methods. Elsevier Academic Press, San Diego

    Google Scholar 

  73. O’Dell TE, Lodge DJ, Mueller GM (2004) Approaches to sampling macrofungi. In: Mueller GM, Bills GF, Foster MS (eds) Biodiversity of fungi - Inventory and monitoring methods. Elsevier Academic Press, San Diego

    Google Scholar 

  74. Ortega-Álvarez R, MacGregor-Fors I (2009) Living in the big city: Effects of urban land-use on bird community structure, diversity, and composition. Landsc Urban Plan 90:189–195

    Article  Google Scholar 

  75. Ortega-Álvarez R, MacGregor-Fors I (2010) What matters most? Relative effect of urban habitat traits and hazards on urban park birds. Ornitol Neotrop 21:519–533

    Google Scholar 

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

    Article  Google Scholar 

  77. Ortega-Álvarez R, Pineda-López R, Pablo-López R, Lindig-Cisneros R, Gómez-Álvarez G, MacGregor-Fors I (2011) Cambio global y urbanización: un enfoque ornitológico. Canto del Centzontle 2:110–111

    Google Scholar 

  78. Pablo-López RE (2009) Primer registro del perico argentino (Myiopsitta monachus) en Oaxaca, México. Huitzil 10:48–51

    Google Scholar 

  79. Pablo-López RE, Díaz-Porras DF (2011) Los campus universitarios como refugios de aves: el caso de la Universidad Autónoma “Benito Juárez” de Oaxaca (UABJO), Oaxaca, México. Canto del Centzontle 2:48–63

    Google Scholar 

  80. Palomino D, Carrascal LM (2007) Threshold distances to nearby cities and roads influence the bird community of a mosaic landscape. Biol Conserv 140:100–109

    Article  Google Scholar 

  81. Pechmann JHK, Wilbur HM (1994) Putting declining amphibian populations in perspective natural fluctuations and human impacts. Herpetologica 50:65–84

    Google Scholar 

  82. Pegler DN (1983) Agaric flora of the Lesser Antilles. Kew Bulletin Additional Series IX. HMSO, London

    Google Scholar 

  83. Pineda-López R, Febvre N, Martínez M (2010) Importancia de proteger pequeñas áreas periurbanas por su riqueza avifaunística: el caso de Mompaní, Querétaro, México. Huitzil 11:69–80

    Google Scholar 

  84. Pollard E, Yates TJ (1993) Monitoring butterflies for ecology and conservation. Chapman and Hall, London

    Google Scholar 

  85. Ralph CJ, Droege S, Sauer JR (1995) Managing and monitoring birds using point counts: Standards and applications. United States Department of Agriculture, Albany

    Google Scholar 

  86. Ramírez-Bastida P, Varona-Graniel DE, DeSucre-Medrano AE (2011) Aves en los relictos de un gran lago: los humedales de la Ciudad de México y áreas vecinas. Canto del Centzontle 2:72–86

    Google Scholar 

  87. Ramírez-Restrepo L (2010) Diversidad de mariposas (Nymphalidae: Biblidinae, Heliconiinae, Itomiinae y Satyrinae) en un mosaico regional de urbanización en Xalapa y Coatepec, Veracruz. Msc Thesis, Instituto de Ecología, A.C., Xalapa, México

    Google Scholar 

  88. Rapoport E, López-Moreno IR (1987) Aportes a la ecología urbana de la Ciudad de México. Limusa, México, D.F.

  89. Ruelas Inzunza E, Aguilar Rodríguez SH (2010) La avifauna urbana del Parque Ecológico Macuiltépetl en Xalapa, Veracruz, México. Ornitol Neotrop 21:87–103

    Google Scholar 

  90. Ruszczyk A, de Mellender Araujo A (1992) Gradients in butterfly species diversity in an urban area in Brazil. J Lepidopt Soc 46:255–264

    Google Scholar 

  91. Sattler T, Pezzatti GB, Nobis MP, Obrist MK, Roth T, Moretti M (2014) Selection of multiple umbrella species for functional and taxonomic diversity to represent urban biodiversity. ConservBiol (doi: 10.1111/cobi.12213)

  92. Sáyago R, MacGregor-Fors I (2010) The arrival of Barn Swallows (Hirundo rustica) to a neotropical city is related to precipitation in wintering areas. Ornitol Neotrop 21:105–108

    Google Scholar 

  93. Soykan CU, Brand LA, Ries L, Stromberg JC, Hass C, Simmons DA, Patterson WJD, Sabo JL (2012) Multitaxonomic diversity patterns along a desert riparian–upland gradient. PLoS ONE 7:e28235

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  94. Vitousek PM, Mooney HA, Lubchenco J, Melillo JM (1997) Human domination of earth’s ecosystems. Science 277:494–499

    Article  CAS  Google Scholar 

  95. Weller B, Ganzhorn JU (2004) Carabid beetle community composition, body size, and fluctuating asymmetry along an urban–rural gradient. Basic ApplEcol 5:193–201

    Article  Google Scholar 

  96. Williams-Linera G, Manson RH, Isuzna EV (2002) La fragmentación del bosque mesófilo de montaña y patrones de uso del suelo en la región oeste de Xalapa, Veracruz, México. Madera Bosques 8:73–89

    Google Scholar 

  97. World Bank (2009) World development report 2009: Reshaping economic geography. Washington, D.C.

  98. Zuria I, Rendón-Hernández G (2010) Notes on the breeding biology of common resident birds in an urbanized area of Hidalgo, Mexico. Huitzil 11:35–41

    Google Scholar 

Download references

Acknowledgments

We are grateful to Richard Lemoine, Emmanuel Arriaga, Martha L. Baena, José Luis Sánchez Huerta, Ángeles Arenas-Cruz, Juan Carlos Corona, David Ramos, Fidel Tapia Padilla, Luis Ángel Espinoza and Miguel A. Domínguez López for their help with field work, specimen identification, and site selection. We also thank the local authorities (Ayuntamiento de Xalapa) for authorizing our survey within the city of Xalapa (Oficio CMA/896/2012). This study was funded by the Dirección General del Instituto de Ecología, A. C. through the “Proyectos de Investigación de Alto Valor Estratégico para la Sociedad” (project: “Patrones ecológicos y percepción social de la diversidad biológica que habita en la ciudad de Xalapa: Un enfoque multidisciplinario”).

Author information

Affiliations

Authors

Corresponding author

Correspondence to Federico Escobar.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

MacGregor-Fors, I., Avendaño-Reyes, S., Bandala, V.M. et al. Multi-taxonomic diversity patterns in a neotropical green city: a rapid biological assessment. Urban Ecosyst 18, 633–647 (2015). https://doi.org/10.1007/s11252-014-0410-z

Download citation

Keywords

  • Urban ecology
  • Mexico
  • Plants
  • Fungi
  • Ants
  • Butterflies
  • Beetles
  • Amphibians
  • Birds