Landscape Ecology

, Volume 34, Issue 7, pp 1825–1836 | Cite as

Small but critical: semi-natural habitat fragments promote bee abundance in cotton agroecosystems across both Brazil and the United States

  • Sarah CusserEmail author
  • Carolina Grando
  • Maria Imaculada Zucchi
  • Margarita M. López-Uribe
  • Nathaniel S. Pope
  • Kimberly Ballare
  • Danielle Luna-Lucena
  • Eduardo A. B. Almeida
  • John L. Neff
  • Kenneth Young
  • Shalene Jha
Research Article



Bees are the most important pollinators of crops worldwide. For most bees, patches of semi-natural habitat within or adjacent to crops can provide important nesting and food resources. Despite this, land cover change is rapidly reducing the abundance of semi-natural habitat within agroecological landscapes, with potentially negative consequences for bee communities and the services they provide.


Identify how the availability of semi-natural habitat impacts bee communities across biogeographic regions, which may reveal commonalities and key governing principles that transcend a single region or taxa.


We analyze and compare the drivers of bee community composition in cotton fields within Brazil and the U.S. to reveal how land cover and land cover change impact bee community composition across these two regions.


We show that the most critical factors impacting bee communities in cotton agroecosystems are the same in Brazil and the U.S.: bee abundance increases with cotton bloom density and the abundance of semi-natural habitat. Further, the loss of semi-natural habitat over a 5-year period negatively impacts bee abundance in both agroecosystems.


Given the importance of bee abundance for the provision of pollination service in cotton plants, our findings highlight the significance of small semi-natural habitat fragments in supporting key ecosystem service providers for both tropical and temperate cotton agroecological systems. We underscore the important role that local land managers play in biodiversity conservation, and the potential contribution they can make to pollination provision by supporting agricultural landscapes that conserve fragments of semi-natural habitat.


Gossypium hirsutum Agroecology Mato Grosso, Brazil Texas, U.S. 



Special thanks to the growers and landowners that allowed us to sample on their lands; without them none of this work would have been possible. For sampling and research permits in Brazil, we thank Chico Mendes Institute for Biodiversity Conservation (ICMBio). This research was supported by the São Paulo Research Foundation (FAPESP—2014/50738-9), The National Council for Scientific and Technological Development (CNPq—310446/2015-5), and the Coordination for the Improvement of Higher Education Personnel CAPES- Programa Biologia Computacional (CAPES-1572813). In the U.S., the help of Texas Agricultural & Mining extension agents, crop consultants, and The Welder Wildlife Foundation, including Roy Parker, Stephen Biles, Lee Hutchins Jr., Kenneth Hanslik, and Terry Blankenship, was invaluable. Thanks to the Jha lab for helpful feedback and support, as well as help in the field from Nicole Vojnovich, Alan Ritchie Jr., Sarah Cunningham, and Rebecca Ruppel. Funding in Texas was provided by the Texas Parks and Wildlife Department, the Army Research Office, and the National Science Foundation.

Supplementary material

10980_2019_868_MOESM1_ESM.docx (29 kb)
Supplementary material 1 (DOCX 29 kb)


  1. Alvarez EC, Plocheck R (2014) Texas Almanac 2014–2015. Texas State Historical Association. Accessed 29 Aug 2017
  2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46Google Scholar
  3. Arino O, Perez JJR, Kalogirou V, Bontemps S, Defourny P, Van Bogaert E (2012) Global land cover map for 2009. ESA & UCLGoogle Scholar
  4. Ashman TL, Knight TM, Steets JA, Amarasekare P, Burd M, Campbell DR, Morgan MT (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421CrossRefGoogle Scholar
  5. Barton K (2016) multi-model inference. R package version 1.15. 6. 2016Google Scholar
  6. Bates D, Mächler M, Bolker B, Walker S (2014) Fitting linear mixed-effects models using lme4. arXiv preprint arXiv:1406.5823
  7. Benton TG, Vickery JA, Wilson JD (2003) Farmland biodiversity: is habitat heterogeneity the key? Trends Ecol Evol 18:182–188CrossRefGoogle Scholar
  8. Biesmeijer JC, Roberts SP, Reemer M, Ohlemüller R, Edwards M, Peeters T, Settele J (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354CrossRefGoogle Scholar
  9. Bommarco R, Lindborg R, Marini L, Öckinger E (2014) Extinction debt for plants and flower-visiting insects in landscapes with contrasting land use history. Divers Distrib 20:591–599CrossRefGoogle Scholar
  10. Brosi BJ, Daily GC, Shih TM, Oviedo F, Durán G (2008) The effects of forest fragmentation on bee communities in tropical countryside. J Appl Ecol 45:773–783CrossRefGoogle Scholar
  11. Burnham KP, Anderson DR (2003) Model selection and multimodel inference: a practical information-theoretic approach. Springer, Fort CollinsGoogle Scholar
  12. Cane JH, Minckley RL, Kervin LJ, Roulston TAH, Williams NM (2006) Complex responses within a desert bee guild (Hymenoptera: Apiformes) to urban habitat fragmentation. Ecol Appl 16:632–644CrossRefGoogle Scholar
  13. Chao A, Chazdon RL, Colwell RK, Shen TJ (2005) A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecol Lett 8:148–159CrossRefGoogle Scholar
  14. Conner WH, Day JW, Baumann RH, Randall JM (1989) Influence of hurricanes on coastal ecosystems along the northern Gulf of Mexico. Wetl Ecol Manag 1:45–56CrossRefGoogle Scholar
  15. Cusser S, Neff JL, Jha S (2015) Land use change and pollinator extinction debt in exurban landscapes. Insect Conserv Divers 8:562–572CrossRefGoogle Scholar
  16. Cusser S, Neff JL, Jha S (2016) Natural land cover drives pollinator abundance and richness, leading to reductions in pollen limitation in cotton agroecosystems. Agric Ecosyst Environ 226:33–42CrossRefGoogle Scholar
  17. Garibaldi LA, Steffan-Dewenter I, Kremen C, Morales JM, Bommarco R, Cunningham SA, Carvalheiro LG, Chacoff NP, Dudenhöffer JH, Greenleaf SS, Holzschuh A (2011) Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol Lett 14:1062–1072CrossRefGoogle Scholar
  18. Ghazoul J (2005) Buzziness as usual? Questioning the global pollination crisis. Trends Ecol Evol 20:367–373CrossRefGoogle Scholar
  19. Ghazoul J (2006) Floral diversity and the facilitation of pollination. J Ecol 94:295–304CrossRefGoogle Scholar
  20. Goulson D (2000) Why do pollinators visit proportionally fewer flowers in large patches? Oikos 91:485–492CrossRefGoogle Scholar
  21. Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1255957CrossRefGoogle Scholar
  22. Grando C, Amon ND, Clough SJ, Guo N, Wei W, Azevedo P, López-Uribe MM, Zucchi MI (2018) Two colors, one species: the case of melissodes nigroaenea (Apidae: Eucerini), an important pollinator of cotton fields in Brazil. Sociobiology 65:645–653CrossRefGoogle Scholar
  23. Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecol 153:589–596CrossRefGoogle Scholar
  24. Grime JP (1998) Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J Ecol 86:902–910CrossRefGoogle Scholar
  25. Han W, Yang Z, Di L, Mueller R (2014) CropScape: a Web service based application for exploring and disseminating US conterminous geospatial cropland data products for decision support. Comput Electron Agric 84:111–123CrossRefGoogle Scholar
  26. Hanski I, Ovaskainen O (2002) Extinction debt at extinction threshold. Conserv Biol 16:666–673CrossRefGoogle Scholar
  27. Hegland SJ, Boeke L (2006) Relationships between the density and diversity of floral resources and flower visitor activity in a temperate grassland community. Ecol Entomol 31:532–538CrossRefGoogle Scholar
  28. Hegland SJ, Grytnes JA, Totland Ø (2009) The relative importance of positive and negative interactions for pollinator attraction in a plant community. Ecol Res 24:929–936CrossRefGoogle Scholar
  29. Helm A, Hanski I, Partel M (2006) Slow response of plant species richness to habitat loss and fragmentation. Ecol Lett 9:72–77Google Scholar
  30. Jha S, Vandermeer JH (2009) Contrasting bee foraging in response to resource scale and local habitat management. Oikos 118:1174–1180CrossRefGoogle Scholar
  31. Kearns CA, Oliveras DM (2009) Environmental factors affecting bee diversity in urban and remote grassland plots in Boulder. Colorado J Insect Conserv 13:655–665CrossRefGoogle Scholar
  32. Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Evol Syst 29:83–112CrossRefGoogle Scholar
  33. Kleijn D, Winfree R, Bartomeus I, Carvalheiro LG, Henry M, Isaacs R, Klein AM, Kremen C, M’gonigle LK, Rader R, Ricketts TH (2015) Delivery of crop pollination services is an insufficient argument for wild pollinator conservation. Nat Commun 6:7414CrossRefGoogle Scholar
  34. Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc Lond 274:303–313CrossRefGoogle Scholar
  35. Krauss J, Bommarco R, Guardiola M, Heikkinen RK, Helm A, Kuussaari M, Steffan Dewenter I (2010) Habitat fragmentation causes immediate and time delayed biodiversity loss at different trophic levels. Ecol Lett 13:597–605CrossRefGoogle Scholar
  36. Kruess A, Tscharntke T (2002) Grazing intensity and the diversity of grasshoppers, butterflies, and trap-nesting bees and wasps. Conserv Biol 16:1570–1580CrossRefGoogle Scholar
  37. Kunin WE (1993) Sex and the single mustard: population density and pollinator behavior effects on seed-set. Ecology 74:2145–2160CrossRefGoogle Scholar
  38. Mato Grosso Institute of Agricultural Economics (2014). Accessed in 12 Oct 2017
  39. McGregor SE (1976) Insect pollination of cultivated crop plants. Agricultural Research Service, US Department of Agriculture, Washington, DCGoogle Scholar
  40. Michener CD (2007) The bees of the world. JHU Press, BaltimoreGoogle Scholar
  41. Myster RW (2016) The physical structure of forests in the Amazon basin: a review. Bot Rev 82:407–427CrossRefGoogle Scholar
  42. Nabhan GP, Buchmann SL (1997) Services provided by pollinators. In: Daily GC (ed) Nature’s Services: societal dependence on natural ecosystems. Island Press, Washington, DC, pp 133–150Google Scholar
  43. Naimi B (2013) usdm: Uncertainty analysis for species distribution models. R package version 1.1-12Google Scholar
  44. O’brien RM (2007) A caution regarding rules of thumb for variance inflation factors. Qual Quant 41:673–690CrossRefGoogle Scholar
  45. Oksanen J, Kindt R, Legendre P, O’Hara B, Stevens MHH, Oksanen MJ (2007) The vegan package. Commun Ecol Package 10:631–637Google Scholar
  46. Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326CrossRefGoogle Scholar
  47. Pedro SRM (2014) The stingless bee fauna in Brazil (Hymenoptera: Apidae). Sociobiology 61:348–354CrossRefGoogle Scholar
  48. Perfecto I, Vandermeer J (2008) Spatial pattern and ecological process in the coffee agroforestry system. Ecology 89:915–920CrossRefGoogle Scholar
  49. Pires VCP, Silveira FA, Sujii ER, Torezani KR, Rodrigues WA, de Albuquerque FA, Rodrigues SM, Salomão AN, Pires CS (2014) Importance of bee pollination for cotton production in conventional and organic farms in Brazil. J Poll Ecol 13:151–160Google Scholar
  50. Pope N, Jha S (2018) Seasonal food scarcity prompts long-distance foraging by a wild social bee. Am Nat 191:45–57CrossRefGoogle Scholar
  51. Potts SG, Vulliamy B, Roberts S, O’Toole C, Dafni A, Ne’eman G, Willmer P (2005) Role of nesting resources in organising diverse bee communities in a Mediterranean landscape. Ecol Entomol 30:78–85CrossRefGoogle Scholar
  52. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353CrossRefGoogle Scholar
  53. QGIS Development Team (2017) QGIS Geographic Information System. Open Source Geospatial Foundation Project.
  54. Ratter JA, Ribeiro JF, Bridgewater S (1997) The Brazilian Cerrado vegetation and threads to its biodiversity. Ann Bot 80:223–230CrossRefGoogle Scholar
  55. Ricketts TH, Regetz J, Steffan-Dewenter I, Cunningham SA, Kremen C, Bogdanski A, Gemmill-Herren B, Greenleaf SS, Klein AM, Mayfield MM, Morandin LA, Ochieng A, Viana BF (2008) Landscape effects on crop pollination services: are there general patterns? Eco Lett 11:499–515CrossRefGoogle Scholar
  56. Roubik DW (1980) Foraging behavior of competing Africanized honeybees and stingless bees. Ecology 61:836–845CrossRefGoogle Scholar
  57. Sang A, Teder T, Helm A, Pärtel M (2010) Indirect evidence for an extinction debt of grassland butterflies half century after habitat loss. Biol Cons 143:1405–1413CrossRefGoogle Scholar
  58. Scialabba NH, Williamson D (2004) The scope of organic agriculture, sustainable forest management and ecoforestry in protected area management. FAO, RomeGoogle Scholar
  59. Thuiller W, Albert C, Araujo MB, Berry PM, Cabeza M, Guisan A, Sykes MT (2008) Predicting global change impacts on plant species’ distributions: future challenges. Perspect Plant Ecol Syst 9:137–152CrossRefGoogle Scholar
  60. Tscharntke T, Klein AM, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity–ecosystem service management. Ecol Lett 8:857–874CrossRefGoogle Scholar
  61. Tylianakis JM, Klein AM, Tscharntke T (2005) Spatiotemporal variation in the diversity of Hymenoptera across a tropical habitat gradient. Ecology 86:3296–3302CrossRefGoogle Scholar
  62. Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363CrossRefGoogle Scholar
  63. Vázquez DP, Morris WF, Jordano P (2005) Interaction frequency as a surrogate for the total effect of animal mutualists on plants. Ecol Lett 8:1088–1094CrossRefGoogle Scholar
  64. Veddeler D, Klein AM, Tscharntke T (2006) Contrasting responses of bee communities to coffee flowering at different spatial scales. Oikos 112:594–601CrossRefGoogle Scholar
  65. Waser NM (1983) The adaptive nature of floral traits: ideas and evidence. Pollinat Biol 1:241–285CrossRefGoogle Scholar
  66. Xie Z, Williams PH, Tang Y (2008) The effect of grazing on bumblebees in the high rangelands of the eastern Tibetan Plateau of Sichuan. Insect Conserv Divers 12:695–703CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Sarah Cusser
    • 1
    Email author
  • Carolina Grando
    • 4
  • Maria Imaculada Zucchi
    • 6
  • Margarita M. López-Uribe
    • 5
  • Nathaniel S. Pope
    • 2
  • Kimberly Ballare
    • 3
  • Danielle Luna-Lucena
    • 7
  • Eduardo A. B. Almeida
    • 8
  • John L. Neff
    • 9
  • Kenneth Young
    • 10
  • Shalene Jha
    • 2
  1. 1.Kellogg Biological StationHickory CornersUSA
  2. 2.Department of Integrative BiologyUniversity of Texas at AustinAustinUSA
  3. 3.Department of Ecology and Evolutionary BiologyUniversity of California Santa CruzSanta CruzUSA
  4. 4.University of Campinas, Institute of BiologyCampinasBrazil
  5. 5.Department of Entomology, Center for Pollinator ResearchPennsylvania State UniversityState CollegeUSA
  6. 6.Agency of Technology in Agribusiness of Sao Paulo State, Secretary of Agriculture and Food Supply of São Paulo StatePiracicabaBrazil
  7. 7.Universidade de São Paulo, Faculdade de Medicina de Ribeirão Preto, Departamento de GenéticaRibeirão PretoBrazil
  8. 8.Universidade de São Paulo, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, Departamento de BiologiaRibeirão PretoBrazil
  9. 9.Central Texas Melittological InstituteAustinUSA
  10. 10.Department of Geography and the EnvironmentUniversity of Texas at AustinAustinUSA

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