The effects of urbanization on bee communities depends on floral resource availability and bee functional traits


Autoři: Caleb J. Wilson aff001;  Mary A. Jamieson aff001
Působiště autorů: Department of Biological Sciences, Oakland University, Rochester, Michigan, United States of America aff001
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: 10.1371/journal.pone.0225852

Souhrn

Wild bees are important pollinators in many ecosystems threatened by anthropogenic disturbance. Urban development can reduce and degrade natural habitat for bees and other pollinators. However, some researchers suggest that cities could also provide refuge for bees, given that agricultural intensification may pose a greater risk. In this study, we surveyed bee communities at 15 farms and gardens across an urban-rural gradient in southeastern Michigan, USA to evaluate the effect of urbanization on bees. We examined how floral resources, bee functional traits, temperature, farm size, and the spatial scale of analysis influence bee response to urbanization. We found that urbanization positively affected bee diversity and evenness but had no effect on total abundance or species richness. Additionally, urbanization altered bee community composition via differential effects on bee species and functional groups. More urbanized sites supported a greater number of exotic, above-ground nesting, and solitary bees, but fewer eusocial bees. Blooming plant species richness positively influenced bee species diversity and richness. Furthermore, the amount of available floral resources was positively associated with exotic and eusocial bee abundances. Across sites, nearly 70% of floral resources were provided by exotic plants, most of which are characterized as weedy but not invasive. Our study demonstrates that urbanization can benefit some bee species and negatively impact others. Notably, Bombus and Lasioglossum (Dialictus), were two important pollinator groups negatively affected by urbanization. Our study supports the idea that urban environments can provide valuable habitat for diverse bee communities, but demonstrates that some bees are vulnerable to urbanization. Finally, while our results indicate that increasing the abundance and richness of floral resources could partially compensate for negative effects of urbanization on bees, the effectiveness of such measures may be limited by other factors, such as urban warming.

Klíčová slova:

Bees – Habitats – Honey bees – Invasive species – Plants – Species diversity – Urban ecology – Urban environments


Zdroje

1. Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, Solter LF, et al. Patterns of widespread decline in North American bumble bees. Proc Natl Acad Sci. 2011;108: 662–667. doi: 10.1073/pnas.1014743108 21199943

2. Goulson D, Nicholls E, Botias C, Rotheray EL. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science (80-). 2015;347: 1255957–1255957. doi: 10.1126/science.1255957 25721506

3. Potts SG, Imperatriz-Fonseca V, Ngo HT, Aizen MA, Biesmeijer JC, Breeze TD, et al. Safeguarding pollinators and their values to human well-being. Nature. 2016;540: 220–229. doi: 10.1038/nature20588 27894123

4. Gallai N, Salles JM, Settele J, Vaissière BE. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ. 2009;68: 810–821. doi: 10.1016/j.ecolecon.2008.06.014

5. Fontaine C, Dajoz I, Meriguet J, Loreau M. Functional Diversity of Plant–Pollinator Interaction Webs Enhances the Persistence of Plant Communities. Waser N, editor. PLoS Biol. 2005;4: e1. doi: 10.1371/journal.pbio.0040001 16332160

6. Biesmeijer JC. Parallel Declines in Pollinators and Insect-Pollinated Plants in Britain and the Netherlands. Science (80-). 2006;313: 351–354. doi: 10.1126/science.1127863 16857940

7. Brown MJF, Paxton RJ. The conservation of bees: a global perspective. Apidologie. 2009;40: 410–416. doi: 10.1051/apido/2009019

8. Kennedy CM, Lonsdorf E, Neel MC, Williams NM, Ricketts TH, Winfree R, et al. A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Anderson M, editor. Ecol Lett. 2013;16: 584–599. doi: 10.1111/ele.12082 23489285

9. Seto KC, Guneralp B, Hutyra LR. Global forecasts of urban expansion to 2030 and direct impacts on biodiversity and carbon pools. Proc Natl Acad Sci. 2012;109: 16083–16088. doi: 10.1073/pnas.1211658109 22988086

10. Matteson KC, Ascher JS, Langellotto GA. Bee Richness and Abundance in New York City Urban Gardens. Ann Entomol Soc Am. 2008;101: 140–150. doi: 10.1603/0013-8746(2008)101[140:BRAAIN]2.0.CO;2

11. Ahrné K, Bengtsson J, Elmqvist T. Bumble Bees (Bombus spp) along a Gradient of Increasing Urbanization. Somers M, editor. PLoS One. 2009;4: e5574. doi: 10.1371/journal.pone.0005574 19440367

12. Bates AJ, Sadler JP, Fairbrass AJ, Falk SJ, Hale JD, Matthews TJ. Changing Bee and Hoverfly Pollinator Assemblages along an Urban-Rural Gradient. Stout JC, editor. PLoS One. 2011;6: e23459. doi: 10.1371/journal.pone.0023459 21858128

13. Geslin B, Le Féon V, Folschweiller M, Flacher F, Carmignac D, Motard E, et al. The proportion of impervious surfaces at the landscape scale structures wild bee assemblages in a densely populated region. Ecol Evol. 2016;6: 6599–6615. doi: 10.1002/ece3.2374 27777733

14. Plascencia M, Philpott SM. Floral abundance, richness, and spatial distribution drive urban garden bee communities. Bull Entomol Res. 2017;107: 658–667. doi: 10.1017/S0007485317000153 28245886

15. Banaszak-Cibicka W, Twerd L, Fliszkiewicz M, Giejdasz K, Langowska A. City parks vs. natural areas—is it possible to preserve a natural level of bee richness and abundance in a city park? Urban Ecosyst. 2018;21: 599–613. doi: 10.1007/s11252-018-0756-8

16. Sirohi MH, Jackson J, Edwards M, Ollerton J. Diversity and abundance of solitary and primitively eusocial bees in an urban centre: a case study from Northampton (England). J Insect Conserv. 2015;19: 487–500. doi: 10.1007/s10841-015-9769-2

17. Theodorou P, Albig K, Radzevičiūtė R, Settele J, Schweiger O, Murray TE, et al. The structure of flower visitor networks in relation to pollination across an agricultural to urban gradient. Kudo G, editor. Funct Ecol. 2017;31: 838–847. doi: 10.1111/1365-2435.12803

18. Baldock KCR, Goddard MA, Hicks DM, Kunin WE, Mitschunas N, Morse H, et al. A systems approach reveals urban pollinator hotspots and conservation opportunities. Nat Ecol Evol. 2019;3: 363–373. doi: 10.1038/s41559-018-0769-y 30643247

19. Dylewski Ł, Maćkowiak Ł, Banaszak-Cibicka W. Are all urban green spaces a favourable habitat for pollinator communities? Bees, butterflies and hoverflies in different urban green areas. Ecol Entomol. 2019; een.12744. doi: 10.1111/een.12744

20. Hall DM, Camilo GR, Tonietto RK, Ollerton J, Ahrné K, Arduser M, et al. The city as a refuge for insect pollinators. Conserv Biol. 2017;31: 24–29. doi: 10.1111/cobi.12840 27624925

21. Cariveau DP, Winfree R. Causes of variation in wild bee responses to anthropogenic drivers. Curr Opin Insect Sci. 2015;10: 104–109. doi: 10.1016/j.cois.2015.05.004 29587998

22. Hernandez JL, Frankie GW, Thorp RW. Ecology of Urban Bees: A Review of Current Knowledge and Directions for Future Study. Cities Environ. 2009;2: 360–376.

23. Baldock KCR, Goddard MA, Hicks DM, Kunin WE, Mitschunas N, Osgathorpe LM, et al. Where is the UK’s pollinator biodiversity? The importance of urban areas for flower-visiting insects. Proc R Soc B Biol Sci. 2015;282: 20142849. doi: 10.1098/rspb.2014.2849 25673686

24. Verboven HAF, Uyttenbroeck R, Brys R, Hermy M. Different responses of bees and hoverflies to land use in an urban-rural gradient show the importance of the nature of the rural land use. Landsc Urban Plan. 2014;126: 31–41. doi: 10.1016/j.landurbplan.2014.02.017

25. Harrison T, Winfree R. Urban drivers of plant-pollinator interactions. Evans K, editor. Funct Ecol. 2015;29: 879–888. doi: 10.1111/1365-2435.12486

26. Winfree R, Bartomeus I, Cariveau DP. Native Pollinators in Anthropogenic Habitats. Annu Rev Ecol Evol Syst. 2011;42: 1–22. doi: 10.1146/annurev-ecolsys-102710-145042

27. Mok H-F, Williamson VG, Grove JR, Burry K, Barker SF, Hamilton AJ. Strawberry fields forever? Urban agriculture in developed countries: a review. Agron Sustain Dev. 2014;34: 21–43. doi: 10.1007/s13593-013-0156-7

28. Brown KH, Jameton AL. Public Health Implications of Urban Agriculture. J Public Health Policy. 2000;21: 20–39. Available: http://www.jstor.org/stable/3343472 10754796

29. Low S, Adalja A, Beaulieu E, Key N, Martinez S, Melton A, et al. Trends in U.S. Local and Regional Food Systems Report to Congress. US Dep Agric Econ Res Serv. 2015.

30. Gardiner MM, Burkman CE, Prajzner SP. The Value of Urban Vacant Land to Support Arthropod Biodiversity and Ecosystem Services. Environ Entomol. 2013;42: 1123–1136. doi: 10.1603/EN12275 24468552

31. Lin BB, Philpott SM, Jha S. The future of urban agriculture and biodiversity-ecosystem services: Challenges and next steps. Basic Appl Ecol. 2015;16: 189–201. doi: 10.1016/j.baae.2015.01.005

32. Matteson KC, Langellotto GA. Bumble Bee Abundance in New York City Community Gardens: Implications for Urban Agriculture. Cities Environ. 2009;2: 1–12. Available: http://digitalcommons.lmu.edu/cate/vol2/iss1/5

33. U.S. Census Bureau PD. Annual Estimates of the Resident Population: April 1, 2010 to July 1, 2017. 2017.

34. Inc. G. Google Earth Pro. Mountainview, CA: Google Inc.; 2017.

35. ESRI. ArcGIS Desktop. Redlands, CA: Environmental Systems Research Institute; 2017.

36. Landis JR, Koch GG. The Measurement of Observer Agreement for Categorical Data. Biometrics. 1977;33: 159–174. 843571

37. Meineke E, Youngsteadt E, Dunn RR, Frank SD. Urban warming reduces aboveground carbon storage. Proc R Soc B Biol Sci. 2016;283: 20161574. doi: 10.1098/rspb.2016.1574 27708149

38. Terando AJ, Youngsteadt E, Meineke EK, Prado SG. Ad hoc instrumentation methods in ecological studies produce highly biased temperature measurements. Ecol Evol. 2017;7: 9890–9904. doi: 10.1002/ece3.3499 29238523

39. Hamblin AL, Youngsteadt E, Frank SD. Wild bee abundance declines with urban warming, regardless of floral density. Urban Ecosyst. 2018;21: 419–428. doi: 10.1007/s11252-018-0731-4

40. USDA N. The PLANTS Database. In: National Plant Data Team, Greensboro, NC. 2019.

41. USDA N. Native, Invasive, and Other Plant-Related Definitions. https://www.nrcs.usda.gov/wps/portal/nrcs/detail/ct/technical/ecoscience/invasive/?cid=nrcs142p2_011124

42. Rhoades P, Griswold T, Waits L, Bosque-Pérez NA, Kennedy CM, Eigenbrode SD. Sampling technique affects detection of habitat factors influencing wild bee communities. J Insect Conserv. 2017;21: 703–714. doi: 10.1007/s10841-017-0013-0

43. Ward K, Cariveau D, May E, Roswell M, Vaughan M, Williams N, et al. Streamlined Bee Monitoring Protocol for Assessing Pollinator Habitat. Portland, OR.; 2014.

44. Tonietto RK, Ascher JS, Larkin DJ. Bee communities along a prairie restoration chronosequence: similar abundance and diversity, distinct composition. Ecol Appl. 2017;27: 705–717. doi: 10.1002/eap.1481 27935661

45. Fortel L, Henry M, Guilbaud L, Guirao AL, Kuhlmann M, Mouret H, et al. Decreasing Abundance, Increasing Diversity and Changing Structure of the Wild Bee Community (Hymenoptera: Anthophila) along an Urbanization Gradient. Smith MA, editor. PLoS One. 2014;9: e104679. doi: 10.1371/journal.pone.0104679 25118722

46. Harrison T, Gibbs J, Winfree R. Phylogenetic homogenization of bee communities across ecoregions. Glob Ecol Biogeogr. 2018;27: 1457–1466. doi: 10.1111/geb.12822

47. Mallinger RE, Gaines-Day HR, Gratton C. Do managed bees have negative effects on wild bees?: A systematic review of the literature. Raine NE, editor. PLoS One. 2017;12: e0189268. doi: 10.1371/journal.pone.0189268 29220412

48. Colwell RK. EstimateS: Statistical Estimation of Species Richness and Shared Species from Samples. Storrs, CT; 2013. http://viceroy.eeb.uconn.edu/estimates/index.html

49. Gotelli NJ, Chao A. Measuring and Estimating Species Richness, Species Diversity, and Biotic Similarity from Sampling Data. Encyclopedia of Biodiversity. Elsevier; 2013. pp. 195–211. doi: 10.1016/B978-0-12-384719-5.00424-X

50. Jost L. Entropy and diversity. Nord Soc Oikos. 2006;113: 363–375. Available: https://www.jstor.org/stable/pdf/40234813.pdf?refreqid=excelsior%3Ae1a0581c7e34c0d5d198fab9a6d25238

51. Jost L. The Relation between Evenness and Diversity. Diversity. 2010;2: 207–232. doi: 10.3390/d2020207

52. GIBBS J, ASCHER JS, RIGHTMYER MG, ISAACS R. The bees of Michigan (Hymenoptera: Apoidea: Anthophila), with notes on distribution, taxonomy, pollination, and natural history. Zootaxa. 2017;4352: 1. doi: 10.11646/zootaxa.4352.1.1 29245534

53. Gibbs J, Brady SG, Kanda K, Danforth BN. Phylogeny of halictine bees supports a shared origin of eusociality for Halictus and Lasioglossum (Apoidea: Anthophila: Halictidae). Mol Phylogenet Evol. 2012;65: 926–939. doi: 10.1016/j.ympev.2012.08.013 22982437

54. Danforth BN, Conway L, Ji S. Phylogeny of Eusocial Lasioglossum Reveals Multiple Losses of Eusociality within a Primitively Eusocial Clade of Bees (Hymenoptera: Halictidae). Syst Biol. 2003;52: 23–36. doi: 10.1080/10635150390132687 12554437

55. Brady SG, Sipes S, Pearson A, Danforth BN. Recent and simultaneous origins of eusociality in halictid bees. Proc R Soc B Biol Sci. 2006;273: 1643–1649. doi: 10.1098/rspb.2006.3496 16769636

56. Team RC. R: A language and environment for statistical computing. Vienna Austria: R Foundation for Statistical Computing; 2018.

57. Ives AR. For testing the significance of regression coefficients, go ahead and log-transform count data. Freckleton R, editor. Methods Ecol Evol. 2015;6: 828–835. doi: 10.1111/2041-210X.12386

58. Okansen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D, et al. Vegan Community Ecology Package Version 2.5–1. 2018. https://cran.r-project.org

59. Gauch HG, Whittaker RH, Wentworth TR. A Comparative Study of Reciprocal Averaging and Other Ordination Techniques. J Ecol. 1977;65: 157–174. Available: https://www.jstor.org/stable/2259071

60. Normandin É, Vereecken NJ, Buddle CM, Fournier V. Taxonomic and functional trait diversity of wild bees in different urban settings. PeerJ. 2017;5: e3051. doi: 10.7717/peerj.3051 28286711

61. Tonietto R, Fant J, Ascher J, Ellis K, Larkin D. A comparison of bee communities of Chicago green roofs, parks and prairies. Landsc Urban Plan. 2011;103: 102–108. doi: 10.1016/j.landurbplan.2011.07.004

62. Cane JH, Minckley RL, Kervin LJ, Roulston TH, Neal M. Complex Responses within a Desert Bee Guild (Hymenoptera: Apiformes) to Urban Habitat Fragmentation. Ecol Appl. 2006;16: 632–644. doi: 10.1890/1051-0761(2006)016[0632:crwadb]2.0.co;2 16711050

63. Carper AL, Adler LS, Warren PS, Irwin RE. Effects of Suburbanization on Forest Bee Communities. Environ Entomol. 2014;43: 253–262. doi: 10.1603/EN13078 24533967

64. Fitch G, Glaum P, Simao M-C, Vaidya C, Matthijs J, Iuliano B, et al. Changes in adult sex ratio in wild bee communities are linked to urbanization. Sci Rep. 2019;9: 3767. doi: 10.1038/s41598-019-39601-8 30842451

65. Velthuis HHW, van Doorn A. A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie. 2006;37: 421–451. doi: 10.1051/apido:2006019

66. Jacobson MM, Tucker EM, Mathiasson ME, Rehan SM. Decline of bumble bees in northeastern North America, with special focus on Bombus terricola. Biol Conserv. 2018;217: 437–445. doi: 10.1016/j.biocon.2017.11.026

67. Goulson D, Lye GC, Darvill B. Decline and Conservation of Bumble Bees. Annu Rev Entomol. 2008;53: 191–208. doi: 10.1146/annurev.ento.53.103106.093454 17803456

68. Wood TJ, Gibbs J, Graham KK, Isaacs R. Narrow pollen diets are associated with declining Midwestern bumble bee species. Ecology. 2019;0. doi: 10.1002/ecy.2697 31012965

69. Minckley RL, Wcislo WT, Yanega D, Stephen L, Buchmann SL. Behavior and Phenology of a Specialist Bee (Dieunomia) and Sunflower (Helianthus) Pollen Availability. Ecology. 1994;75: 1406–1419.

70. Peterson JH, Roitberg BD, Peterson JH. Impacts of flight distance on sex ratio and resource allocation to offspring in the leafcutter bee, Megachile rotundata. Behav Ecol Sociobiol. 2006;59: 589–596. doi: 10.1007/s00265-005-0085-9

71. Suzuki Y, Kawaguchi LG, Munidasa DT, Toquenaga Y. Do bumble bee queens choose nest sites to maximize foraging rate? Testing models of nest site selection. Behav Ecol Sociobiol. 2009;63: 1353–1362. doi: 10.1007/s00265-009-0789-3

72. Kaluza BF, Wallace HM, Heard TA, Minden V, Klein A, Leonhardt SD. Social bees are fitter in more biodiverse environments. Sci Rep. 2018;8: 12353. doi: 10.1038/s41598-018-30126-0 30120304

73. Simao M-CM, Matthijs J, Perfecto I. Experimental small-scale flower patches increase species density but not abundance of small urban bees. Beggs J, editor. J Appl Ecol. 2018;55: 1759–1768. doi: 10.1111/1365-2664.13085

74. Blackmore LM, Goulson D. Evaluating the effectiveness of wildflower seed mixes for boosting floral diversity and bumblebee and hoverfly abundance in urban areas. Stewart A, Bezemer M, editors. Insect Conserv Divers. 2014;7: 480–484. doi: 10.1111/icad.12071

75. Matteson KC, Langellotto GA. Determinates of inner city butterfly and bee species richness. Urban Ecosyst. 2010;13: 333–347. doi: 10.1007/s11252-010-0122-y

76. Hülsmann M, von Wehrden H, Klein A-M, Leonhardt SD. Plant diversity and composition compensate for negative effects of urbanization on foraging bumble bees. Apidologie. 2015;46: 760–770. doi: 10.1007/s13592-015-0366-x

77. Threlfall CG, Walker K, Williams NSG, Hahs AK, Mata L, Stork N, et al. The conservation value of urban green space habitats for Australian native bee communities. Biol Conserv. 2015;187: 240–248. doi: 10.1016/j.biocon.2015.05.003

78. Bennett AB, Lovell S. Landscape and local site variables differentially influence pollinators and pollination services in urban agricultural sites. Zang R, editor. PLoS One. 2019;14: e0212034. doi: 10.1371/journal.pone.0212034 30759171

79. Mach BM, Potter DA. Quantifying bee assemblages and attractiveness of flowering woody landscape plants for urban pollinator conservation. Puebla I, editor. PLoS One. 2018;13: e0208428. doi: 10.1371/journal.pone.0208428 30586408

80. Salisbury A, Armitage J, Bostock H, Perry J, Tatchell M, Thompson K. EDITOR’S CHOICE: Enhancing gardens as habitats for flower-visiting aerial insects (pollinators): should we plant native or exotic species? Diamond S, editor. J Appl Ecol. 2015;52: 1156–1164. doi: 10.1111/1365-2664.12499

81. Williams NM, Cariveau D, Winfree R, Kremen C. Bees in disturbed habitats use, but do not prefer, alien plants. Basic Appl Ecol. 2011;12: 332–341. doi: 10.1016/j.baae.2010.11.008

82. Chrobock T, Winiger P, Fischer M, van Kleunen M. The cobblers stick to their lasts: pollinators prefer native over alien plant species in a multi-species experiment. Biol Invasions. 2013;15: 2577–2588. doi: 10.1007/s10530-013-0474-3

83. FUKASE J. INCREASED POLLINATOR ACTIVITY IN URBAN GARDENS WITH MORE NATIVE FLORA. Appl Ecol Environ Res. 2016;14: 297–310. doi: 10.15666/aeer/1401_297310

84. Ballard M, Hough-Goldstein J, Tallamy D. Arthropod Communities on Native and Nonnative Early Successional Plants. Environ Entomol. 2013;42: 851–859. doi: 10.1603/EN12315 24331597

85. Burghardt KT, Tallamy DW, Philips C, Shropshire KJ. Non-native plants reduce abundance, richness, and host specialization in lepidopteran communities. Ecosphere. 2010;1: art11. doi: 10.1890/ES10-00032.1

86. Burghardt KT, Tallamy DW. Plant origin asymmetrically impacts feeding guilds and life stages driving community structure of herbivorous arthropods. van Kleunen M, editor. Divers Distrib. 2013;19: 1553–1565. doi: 10.1111/ddi.12122

87. Pyšek P. Alien and native species in central European urban floras: a quantitative comparison. J Biogeogr. 1998;25: 155–163. Available: https://www.jstor.org/stable/pdf/2846284.pdf

88. Perre P, Loyola RD, Lewinsohn TM, Almeida-Neto M. Insects on urban plants: contrasting the flower head feeding assemblages on native and exotic hosts. Urban Ecosyst. 2011;14: 711–722. doi: 10.1007/s11252-011-0179-2

89. Hinners SJ, Hjelmroos-Koski MK. Receptiveness of Foraging Wild Bees to Exotic Landscape Elements. Am Midl Nat. 2009;162: 253–265. Available: https://www.jstor.org/stable/25602317

90. Theodorou P, Radzevičiūtė R, Settele J, Schweiger O, Murray TE, Paxton RJ. Pollination services enhanced with urbanization despite increasing pollinator parasitism. Proc R Soc B Biol Sci. 2016;283: 20160561. doi: 10.1098/rspb.2016.0561 27335419

91. Osborne JL, Martin AP, Shortall CR, Todd AD, Goulson D, Knight ME, et al. Quantifying and comparing bumblebee nest densities in gardens and countryside habitats. J Appl Ecol. 2007;45: 784–792. doi: 10.1111/j.1365-2664.2007.01359.x

92. McFrederick QS, LeBuhn G. Are urban parks refuges for bumble bees Bombus spp. (Hymenoptera: Apidae)? Biol Conserv. 2006;129: 372–382. doi: 10.1016/j.biocon.2005.11.004

93. Glaum P, Simao M-C, Vaidya C, Fitch G, Iulinao B. 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. 2017;4: 170156. doi: 10.1098/rsos.170156 28573023

94. Lahr EC, Dunn RR, Frank SD. Getting ahead of the curve: cities as surrogates for global change. Proc R Soc B Biol Sci. 2018;285: 20180643. doi: 10.1098/rspb.2018.0643

95. Hamblin AL, Youngsteadt E, López-Uribe MM, Frank SD. Physiological thermal limits predict differential responses of bees to urban heat-island effects. Biol Lett. 2017;13: 20170125. doi: 10.1098/rsbl.2017.0125 28637837

96. Jamieson MA, Carper AL, Wilson CJ, Scott VL, Gibbs J. Geographic Biases in Bee Research Limits Understanding of Species Distribution and Response to Anthropogenic Disturbance. Front Ecol Evol. 2019;7: 1–8. doi: 10.3389/fevo.2019.00194

97. Archer CR, Pirk CWW, Carvalheiro LG, Nicolson SW. Economic and ecological implications of geographic bias in pollinator ecology in the light of pollinator declines. Oikos. 2014;123: 401–407. doi: 10.1111/j.1600-0706.2013.00949.x


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