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Combining phylogeography and future climate change for conservation of Bombus morio and B. pauloensis (Hymenoptera: Apidae)

  • Elaine Françoso
  • Alexandre Rizzo Zuntini
  • Maria Cristina Arias
ORIGINAL PAPER

Abstract

A worldwide decline of many bee species has been reported, but conversely some species seems to be in expansion. Nonetheless species truly in expansion may be overestimated, especially when they are considered as a whole, and information about intraspecific lineages is lacking. The objective of this study was to test whether the bumblebee species Bombus morio and B. pauloensis will be safe under future climate changes. Specifically, test if these bees will suffer geographic decline or expansion; test whether each phylogeographic lineage within B. pauloensis will respond differently in modeling of future geographic distribution given climate change; find stable areas holding high genetic diversity based on predicted future climatic changes; and test whether these areas are covered by existing protected areas. To reach the objectives we performed analyses using phylogeographic data already available and climate change information to model the demography of the panmictic B. morio and the phylogeographic lineages in B. pauloensis. Our results suggest that both species will suffer a reduction in suitable area and that the reduction in distribution is masked for B. pauloensis. When each clade was separately analyzed, the ones in the edge of the species distribution are the most likely to decline. We found a large future refuge in eastern state of São Paulo and state of Rio de Janeiro for B. morio and for the clades of B. pauloensis. This refuge seems to show high levels of species richness and endemism for different taxa. Thus, by protecting this area we will be preserving not only the pattern of biodiversity but also the processes that generate and maintain them for many other species.

Keywords

Phylogeographic lineages Future distribution modeling Conservation Bumblebee Brazil 

Notes

Acknowledgements

We would like to thank J. Richard Abbott for English review of the earlier version of the manuscript, the Missouri Botanical Garden (Saint Louis, MO, USA) where this manuscript was written, Flavio de Oliveira Francisco for comments, and Susy Coelho for the laboratory maintenance. Financial support was provided by Fundação de Amparo à Pesquisa do Estado de São Paulo (Proc. 10/50597-5 and 13/12530-4; Ph.D. and scholarship to EF 2009/07124-1, 2010/20548-2 and 2013/03961-1) and by Conselho Nacional de Desenvolvimento Científico e Tecnológico (research fellowship to MCA).

Author contributions

EF, did the research and wrote the manuscript; ARZ, assistance in data analysis, R scripts and advice; and MCA, advice, guidance and support in preparing the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare no potential conflict of interests.

Supplementary material

10841_2018_114_MOESM1_ESM.xlsx (238 kb)
Supplementary material 1 (XLSX 238 KB)
10841_2018_114_MOESM2_ESM.pdf (287.1 mb)
Supplementary material 2 (PDF 293952 KB)

References

  1. Aldana J, Cure JR, Almanza MT, Vecil D, Rodríguez D (2007) Efecto de Bombus atratus (Hymenoptera: Apidae) sobre la productividad de tomate (Lycopersicon esculentum Mill.) bajo invernadero en la Sabana de Bogotá, Colombia. Agron Colomb 25:62–72Google Scholar
  2. Ascher JS, Pickering J (2014) Discover life bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila). http://www.discoverlife.org/mp/20qguide=Apoidea_species. Accessed 21 Feb 2017
  3. Batra WT (1995) Bees and pollination in our changing environment. Apidologie 26:361–370CrossRefGoogle Scholar
  4. 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 313:351–354CrossRefPubMedGoogle Scholar
  5. Bivand R, Lewin-Koh N (2013) Maptools: tools for reading and handling spatial objects. R package version 0, pp 8–27. http://CRAN.Rproject.org/package=maptools
  6. Bivand R, Rundel C (2014) rgeos: interface to geometry engine—open source (GEOS). R package version 0.3-5. http://CRAN.R-project.org/package=rgeos
  7. Bivand R, Keitt T, Rowlingson B (2013) rgdal: bindings for the geospatial data. R package version 0.8-13. http://CRAN.R-project.org/package=rgdaland
  8. Buttermore RE (1997) Observations of successful Bombus terrestris (L.) (Hymenoptera: Apidae) colonies in southern Tasmania. Aust J Entomol 36:251–254CrossRefGoogle Scholar
  9. Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, Solter LF, Griswold TL (2011) Patterns of widespread decline in North American bumble bees. Proc Natl Acad Sci USA 108:662–667CrossRefPubMedGoogle Scholar
  10. Cane JH, Tepedino VJ (2001) Causes and extent of declines among native North American invertebrate pollinators: detection, evidence, and consequences. Conserv Ecol 5:1CrossRefGoogle Scholar
  11. Carvell C (2002) Habitat use and conservation of bumblebees (Bombus spp.) under different grassland management regimes. Biol Conserv 103:33–49CrossRefGoogle Scholar
  12. Colla SR, Packer L (2008) Evidence for decline in eastern North American bumblebees (Hymenoptera: Apidea), with special focus on Bombus affinis Cresson. Biodivers Conserv 17:1379–1391CrossRefGoogle Scholar
  13. Corbet SA, Williams IH, Osborne JL (1991) Bees and the pollination of crops and wildflowers in the European community. Bee World 72:47–49CrossRefGoogle Scholar
  14. Costa LP, Leite YLR, da Fonseca GAB, da Fonseca MT (2000) Biogeography of South American forest mammals: endemism and diversity in the Atlantic forest. Biotropica 32:872–881CrossRefGoogle Scholar
  15. D’Amen M, Zimmermann NE, Pearman PB (2013) Conservation of phylogeographic lineages under climate change. Global Ecol Biogeogr 22:93–104CrossRefGoogle Scholar
  16. D’Avila M, Marchini LC (2005) Polinização realizada por abelhas em culturas de importância econômica do Brasil. Bol Ind Anim 62:79–90Google Scholar
  17. da Silva JMC, de Sousa MC, Castelletti CHM (2004) Areas of endemism for passerine birds in the Atlantic forest, South America. Glob Ecol Biogeogr 13:85–92CrossRefGoogle Scholar
  18. da Silveira TMT, Raseira MCB, Nava DE, Couto M (2011) Blueberry pollination in southern Brazil and their influence on fruit quality. Rev Bras Frutic 33:81–88CrossRefGoogle Scholar
  19. De la Rúa P, Jaffé R, Dall’Olio R, Muñoz I, Serrano J (2009) Biodiversity, conservation and current threats to European honeybees. Apidologie 40:263–284CrossRefGoogle Scholar
  20. Doherty PF, Boulinier T, Nichols JD (2003) Local extinction and turnover rates at the edge and interior of species’ ranges. Ann Bot Fenn 40:145–153Google Scholar
  21. Elith J, Graham CH, Anderson RP, Dudík M, Ferrier S, Guisan A, Hijmans RJ, Huettmann F, Leathwick JR, Lehmann A, Li J, Lohmann LG, Loiselle BA, Manion G, Moritz C, Nakamura M, Nakazawa Y, McC. Overton J, Peterson AT, Phillips SJ, Richardson K, Scachetti-Pereira R, Schapire RE, Soberón J, William S, Wisz MS, Zimmermann NE (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29:129–151CrossRefGoogle Scholar
  22. Ellis JS, Knight ME, Darvill B, Goulson D (2006) Extremely low effective population sizes, genetic structuring and reduced genetic diversity in a threatened bumblebee species, Bombus sylvarum (Hymenoptera: Apidae). Mol Ecol 15:4375–4386CrossRefPubMedGoogle Scholar
  23. Fitzpatrick U, Murray MG, Paxton RJ, Breen J, Cotton D, Santorum V, Brown MJF (2007) Rarity and decline in bumblebees—a test of causes and correlates in the Irish fauna. Biol Conserv 136:185–194CrossRefGoogle Scholar
  24. Fontaine C, Dajoz I, Meriguet J, Loreau M (2006) Functional diversity of plant–pollinator interaction webs enhances the persistence of plant communities. PLoS Biol 4:e1CrossRefPubMedGoogle Scholar
  25. Francisco FO, Santiago LR, Mizusawa YM, Oldroyd BP, Arias MC (2016) Genetic structure of island and mainland population of a neotropical bumble bee species. J Insect Conserv 20:383–394CrossRefGoogle Scholar
  26. Françoso E, Zuntini AR, Carnaval AC, Arias MC (2016a) Comparative phyleogeography in the Atlantic forest and Brazilian savannas: pleistocene fluctuations and dispersal shape the spatial patterns in two bumblebees. BMC Evol Biol 6:267CrossRefGoogle Scholar
  27. Françoso E, Oliveira FF, Arias MC (2016b) An integrative approach identifies a new species of bumblebee (Hymenoptera: Apidae: Bombini) from northeastern Brazil. Apidologie 47:171–185CrossRefGoogle Scholar
  28. Giannini TC, Acosta AL, Garófalo CA, Saraiva AM, Alves-dos-Santos I, Imperatriz-Fonseca VL (2012) Pollination services at risk: bee habitats will decrease owing to climate change in Brazil. Ecol Model 244:127–131CrossRefGoogle Scholar
  29. Giannini TC, Boff S, Cordeiro GD, Cartolano EA Jr, Veiga AK, Imperatriz-Fonseca VL, Saraiva AM (2015) Crop pollinators in Brazil: a review of reported interactions. Apidologie 46:209–223CrossRefGoogle Scholar
  30. Goulson D (2006) The demise of the bumblebee in Britain. Biologist 53:294–299Google Scholar
  31. Goulson D (2010) Bumblebees: behavior, ecology, and conservation, 2nd edn. Oxford University Press, OxfordGoogle Scholar
  32. Goulson D, Lye GC, Darvil B (2008) Decline and conservation of bumble bees. Annu Rev Entomol 53:191–208CrossRefPubMedGoogle Scholar
  33. Grixti JC, Wong LT, Cameron SA, Favret C (2009) Decline of bumble bees (Bombus) in the North American Midwest. Biol Conserv 142:75–84CrossRefGoogle Scholar
  34. Hannah L, Midgley GF, Lovejoy T, Bonds WJ, Bush M, Lovett JC, Scott D, Woodward FI (2002) Conservation of biodiversity in a changing climate. Conserv Biol 16:264–268CrossRefGoogle Scholar
  35. Hijmans RJ (2014a) Raster: geographic data analysis and modeling. R package version 2.2-12. http://CRAN.R-project.org/package=raster
  36. Hijmans RJ (2014b) Geosphere: spherical trigonometry. R package version 1.3-11. http://CRAN.R-project.org/package=geosphere
  37. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978CrossRefGoogle Scholar
  38. Kerr JT, Pindar A, Galpern P, Packer L, Potts SG, Roberts SM, Rasmont P, Schweiger O, Colla SR, Richardson LL, Wagner DL, Gall LF, Sikes DS, Pantoja A (2015) Climate change impacts on bumblebees converge across continents. Science 349:177–180CrossRefPubMedGoogle Scholar
  39. Kevan PG (1991) Pollination: keystone process in sustainable global productivity. Acta Hort 288:103–110CrossRefGoogle Scholar
  40. Kosior A, Celary W, Olejniczak P, Fijat J, Król W, Solarz W, Plonka P (2007) The decline of the bumble bees and cockoo bees (Hymenoptera: Apidae: Bombini) of Western and Central Europe. Oryx 41:79–88CrossRefGoogle Scholar
  41. Kramer K, Degen B, Buschbom J, Hickler T, Thuiller W, Sykes M, Winter W (2010) Modelling exploration of the future of European beech (Fagus sylvatica L.) under climate change-range, abundance, genetic diversity and adaptive response. Forest Ecol Manag 259:2213–2222CrossRefGoogle Scholar
  42. Kraus FB, Wolf S, Moritz RF (2009) Male flight distance and population substructure in the bumblebee Bombus terrestris. J Anim Ecol 78:247–252CrossRefPubMedGoogle Scholar
  43. Kremen C, Cameron A, Moilanen A, Phillips SJ, Thomas CD, Beentje H, Dransfield J, Fisher BL, Glaw F, Good TC, Harper GJ, Hijmans RJ, Lees DC, Louis E Jr, Nussbaum RA, Raxworthy CJ, Razafimpahanana A, Schatz GE, Vences M, Vieites DR, Wright PC, Zjhra ML (2008) Aligning conservation priorities across taxa in Madagascar with high-resolution planning tools. Science 320:222–226CrossRefPubMedGoogle Scholar
  44. Lepais O, Darvill B, O`Connor S, Osborne JL, Sanderson RA, Cussans J, Goffe L, Goulson D (2010) Estimation of bumblebee queen dispersal distances using sibship reconstruction method. Mol Ecol 19:819–831CrossRefPubMedGoogle Scholar
  45. Lira-Noriega A, Manthey JD (2013) Relationship of genetic diversity and niche centrality: a survey and analysis. Evolution 68:1082–1093CrossRefGoogle Scholar
  46. Loiselle BA, Graham CH, Goerck JM, Ribeiro MC (2010) Assessing the impact of deforestation and climate change on the range size and environmental niche of bird species in the Atlantic forests, Brazil. J Biogeogr 37:1288–1301CrossRefGoogle Scholar
  47. Lozier JD, Cameron SA (2009) Comparative genetic analyses of historical and contemporary collections highlight contrasting demographic histories for the bumble bees Bombus pensylvanicus and B. impatiens in Illinois. Mol Ecol 18:1875–1886CrossRefPubMedGoogle Scholar
  48. Lozier JD, Strange JP, Stewart IJ, Cameron SA (2011) Patterns of range-wide genetic variation in six North American bumble bee (Apidae: Bombus) species. Mol Ecol 20:4870–4888CrossRefPubMedGoogle Scholar
  49. Macfarlane RP (1995) Distribution of bumble bees in New Zealand. N Z Entomol 8:29–36CrossRefGoogle Scholar
  50. Maiorano L, Falcucci A, Zimmermann NE, Psomas A, Pottier J, Baisero D, Rondinini C, Guisan A, Boitani L (2011) The future of terrestrial mammals in the Mediterranean basin under climate change. Philos Trans R Soc B 366:2681–2692CrossRefGoogle Scholar
  51. Martins AC, Melo GAR (2010) Has the bumblebee Bombus bellicosus gone extinct in the northern portion of its distribution range in Brazil? J Insect Conserv 14:207–210CrossRefGoogle Scholar
  52. Martins AC, Silva DP, De Marco Jr P, Melo GAR (2015) Species conservation under future climate change: the case of Bombus bellicosus, a potentially threatened South American bumble bee species. J Insect Conserv 19:33–43CrossRefGoogle Scholar
  53. Maués MM (2002) Reproductive phenology and pollination of the Brazil nut tree (Bertholletia excelsa Humb. and Bonpl. Lecythidaceae) in estern Amazonia. In: Kevan P, Imperatriz Fonseca VL (eds) Pollinating bees—the conservation link between agriculture and nature. Ministry of Environment, Brasília, pp 245–254Google Scholar
  54. McFrederick Q, LeBuhn G (2006) Are urban parks refuges for bumble bees Bombus spp. (Hymenoptera: Apidae)? Biol Conserv 129:372–382CrossRefGoogle Scholar
  55. Memmott J, Waser NM, Price MV (2004) Tolerance of pollination networks to species extinctions. Proc R Soc Lond B 271:2605–2611CrossRefGoogle Scholar
  56. Montemor KA, Souza DTM (2009) Biodiversidade de polinizadores e biologia floral em cultura de berinjela (Solanum melongena). Zootec Trop 27:97–103Google Scholar
  57. Morales CL, Arbetman MP, Cameron SA, Aizen MA (2013) Rapid ecological replacement of a native bumble bee by invasive species. Front Ecol Environ 11:529–534CrossRefGoogle Scholar
  58. Moritz C (1994) Defining ‘evolutionary significant units’ for conservation. Trends Ecol Evol 9:373–375CrossRefGoogle Scholar
  59. Moure JS, Sakagami SF (1962) As mamangabas sociais do Brasil (Bombus Latreille) (Hymenoptera, Apoidea). Stud Entomol 5:65–194Google Scholar
  60. Olesen JM, Bascompte J, Dupont YL, Jordano P (2007) The modularity of pollination networks. Proc Natl Acad Sci USA 104:19891–19896CrossRefPubMedGoogle Scholar
  61. Pauw A (2007) Collapse of a pollination web in small conservation areas. Ecology 88:1759–1769CrossRefPubMedGoogle Scholar
  62. Pearce JL, Ferrier S (2000) An evaluation of alternative algorithms for fitting species distribution models using logistic regression. Ecol Model 128:127–147CrossRefGoogle Scholar
  63. Pearman PB, D’Amen M, Graham CH, Thuiller W, Zimmermann N (2010) Within-taxon niche structure: niche conservatism, divergence and predicted effects of climate change. Ecography 33:990–1003CrossRefGoogle Scholar
  64. Petit RJ, Mousadik AE, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855CrossRefGoogle Scholar
  65. Phillips SJ, Dudik M (2008) Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31:161–175CrossRefGoogle Scholar
  66. Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259CrossRefGoogle Scholar
  67. Pinto-da-Rocha R, da Silva MB, Bragagnolo C (2005) Faunistic similarity and historic biogeography of the harvestmen of southern and southeastern Atlantic Rain Forest of Brazil. J Arachnol 33:290–299CrossRefGoogle Scholar
  68. Porto TJ, Carnaval AC, da Rocha PLB (2013) Evaluating refugial models using species distribution models, model filling and inclusion: a case study with 14 Brazilian species. Divers Distrib 19:330–340CrossRefGoogle Scholar
  69. 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 40:220–229CrossRefGoogle Scholar
  70. Pywell RF, Warman EA, Hulmes L, Hulmes S, Nuttall P, Sparks TH, Critchley CNR, Sherwood A (2006) Effectiveness of new agri-environment schemes in providing foraging resources for bumble bees in intensively farmed landscapes. Biol Conserv 129:192–206CrossRefGoogle Scholar
  71. R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna. http://www.R-project.org/
  72. Ribeiro MC, Metzger JP, Martensen AC, Ponzono FG, Hirota MM (2009) The Brazilian Atlantic Forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153CrossRefGoogle Scholar
  73. Ridley M (2004) Evolution, 3rd edn. Blackwell Publishing, TurinGoogle Scholar
  74. Santos JE, Santos FR, Silveira FA (2015) Hitting an unintended target: Phylogeography of Bombus brasiliensis Lepeletier, 1836 and the first new Braziliam bumblebee species in a century (Hymenoptera: Apidae). PLoS ONE 10:e0125847CrossRefPubMedPubMedCentralGoogle Scholar
  75. Saupe EE, Papes M, Selden PA, Vetter RS (2011) Tracking a medically important spider: climate change, ecological niche modeling, and the brown recluse (Loxosceles reclusa). PLoS ONE 6:e17731CrossRefPubMedPubMedCentralGoogle Scholar
  76. Smith TB, Kark S, Schneider CJ, Wayne RK, Moritz C (2001) Biodiversity hotspots and beyond: the need for preserving environmental transitions. Trends Ecol Evol 16:431CrossRefGoogle Scholar
  77. Taubmann J, Theissinger K, Feldheim KA, Laube I, Graf W, Haase P, Johannesen J, Pauls SU (2011) Modelling range shifts and assessing genetic diversity distribution of the montane aquatic mayfly Ameletus inopinatus in Europe under climate change scenarios. Conserv Genet 12:503–515CrossRefGoogle Scholar
  78. Thuiller W, Lavergne S, Roquet C, Boulangeat I, Lafourcade B, Araujo MB (2011) Consequences of climate change on the tree of life in Europe. Nature 470:531–534CrossRefPubMedGoogle Scholar
  79. Vamosi JC, Knight TM, Steets JA, Mazer SJ, Burd M, Ashman TL (2006) Pollination decays in biodiversity hotspots. Proc Natl Acad Sci USA 103:956–961CrossRefPubMedGoogle Scholar
  80. Velthuis HHW, van Doorn A (2006) A century of advances in bumblebee domestication and the economic and environmental aspects of commercialization for pollination. Apidologie 37:421–451CrossRefGoogle Scholar
  81. Watt MS, Stone JK, Hood IA, Manning LK (2011) Using a climatic niche model to predict the direct and indirect impacts of climate change on the distribution of Douglas-fir in New Zealand. Glob Change Biol 17:3608–3619CrossRefGoogle Scholar
  82. Williams PH (1982) The distribution and decline of British bumble bees (Bombus Latr.). J Apic Res 21:236–245CrossRefGoogle Scholar
  83. Williams PH (1986) Environmental change and the distribution of British bumble bees (Bombus Latr.). Bee World 67:50–61CrossRefGoogle Scholar
  84. Williams PH (1988) Habitat use by bumble bees (Bombus spp.). Ecol Entomol 13:223–237CrossRefGoogle Scholar
  85. Williams PH, Osborne JL (2009) Bumblebee vulnerability and conservation world-wide. Apidologie 40:367–387CrossRefGoogle Scholar
  86. Williams PH, Colla S, Xie Z-H (2009) Bumblebee vulnerability: common correlates of winners and losers across three continents. Conserv Biol 23:931–940CrossRefPubMedGoogle Scholar
  87. Yamamoto M, da Silva CI, Augusto SC, Barbosa AAA, Oliveira PE (2012) The role of bee diversity in pollination and fruit set of yellow passion fruit (Passiflora edulis forma flavicarpa, Passifloraceae) crop in Central Brazil. Apidologie 43:515–526CrossRefGoogle Scholar
  88. Zayed A (2009) Bee genetics and conservation. Apidologie 40:237–262CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Elaine Françoso
    • 1
  • Alexandre Rizzo Zuntini
    • 2
  • Maria Cristina Arias
    • 1
  1. 1.Instituto de BiociênciasUniversidade de São PauloSão PauloBrazil
  2. 2.Instituto de BiologiaUniversidade Estadual de CampinasCampinasBrazil

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